By Rhawn Joseph, Ph.D.
by Rhawn Joseph, Ph.D. THE EVOLUTION OF THE BRAIN EVOLUTION
The Neuron, Nerve Net, Limbic System, Brainstem, Midbrain, Diencephalon, Striatum, & Telencephalon
Seven hundred million years after the Earth was formed and over the ensuing three hundred million years, single celled organisms began to proliferate within the crust of the Earth and throughout the primeval ocean and salty seas (Mojzsis, et al., 1996; Schopf, 1993; Woese et al., 1990). These single celled creatures appear to have been DNA-equipped and appear to have included organisms which were able to engage in photosynthesis (photoautotrophs), those who could digest minerals, ores and inorganic chemicals (chemoautotrophs), and those which fed off the organic molecules secreted by these other species (heterotrophs). Be it sunlight, miners, or organic molecules, these energy sources provided them with energy, enabled them to survive, and provided evidence of their passing. For example, the oldest sedimentary and volcanic rocks, which are 3.8 billion years in age, contain a surplus of a specific carbon isotope (12C) which is produced during the course of photosynthesis (Mojzsis, 1996). Hence it appears that photosynthesizing life forms had taken up residence on Earth within just a few hundred million years after it had formed.
By 3.46 billion years ago (Schopf, 1993) blue green algae, archaea and creatures resembling modern day cyanobacteria began to overrun the planet. These anaerobes were perfectly adapted for life on a world continually bathed in ultra-violent radiation and lacking free-oxygen. These microbes secreted and coated themselves with a glue-like gelatinous substance which protected them from ultraviolet rays. In fact, By 3.46 billion years B.P., gel-secreting, photosynthesizing cyanobacterial communities were constructing stomatolites ("stone mattresses"), upon the surface layers of shallow seas. These layered structures have been discovered on every continent within sedimentary limestone; hence they either emerged multi-regionally or rapidly dispersed throughout the world. Moreover, microfossils have been discovered in association with the oldest of these stromatolites, dated to 3.5 billion years B.P., in Western Australia (Schopf, 1993).
Exceedingly complex single cell prokaryotes (Mojzsis, et al., 1996; Schopf, 1993) and possibly eukaryotes (Woese, 1989, Woese et al., 1990) had therefore gained dominion over the planet well over 3 billion years ago. As is apparent from the fossil evidence, the cellular contents of these creatures, including their DNA, was protected by a semi-permeable membrane which allowed them to maintain their own internal atmosphere of fluids and essential elements. This porous membrane also enabled these organisms to discharge waste products and to secrete mineral digesting enzymes and mineral creating enzymes, as well as absorb chemical nutrients arising in the external environment (e.g., chemoautotrophs). Moreover, these organisms were able to secrete or detect material released by other single celled creatures (e.g., heterotrophs), such that, at a very rudimentary level, these cells were able to sense, acquire, store, activate, and exchange information in a meaningful fashion.
As is evident from an examination of 3.5 billion year old stromatolites, single celled creatures were able to communicate and engage in cooperative efforts so as to act collectively. Presumably this initial means of singled celled cooperative communication took place via chemical secretions and electrical discharges and alterations in membrane polarity and electric currents (e.g., Bishop, 1956; Clayton, 1979). For example, it is well known that the surface membrain of a living cell is maintained by electrical forces and the interactions between macro-molecules. and that positively charged areas on one molecule are attracted to the negatively charged surface of a different molecule. Moreover, alterations in membrane polarization result in alterations in excitability which are translated into different membrane currents and discharge patterns. Hence, via alterations in these electrical-magnetic forces, molecular cellular structures are able to approach, position themselves, interact and even exchange material and then separate.
That these ancient DNA-equipped creatures were able to function and communicate in this manner, especially via electrical impulses, is also suggested by the nature of DNA which is able to conduct electrical current. Specifically, it has been demonstrated that "the resistivity values derived... are comparable to those of conducting polymers, and indicate that DNA transports electrical current as efficiently as a good semiconductor. DNA is ideally suited for the construction of mesoscopic electronic devices" (Fink & Schonenberger, 1999, p. 407).
In that the most primitive means of true nerve cell communication also occurs via electrical and electro-chemical interactions, whereas true neuronal actions and neuronal circuit activity are also determined by membrane currents, it is therefore quite likely that these early single celled communicative and cooperative efforts were the harbingers of advances in communication yet to come; i.e. the evolution of the neuron.
However, the first neurons probably did not arise until after the planet became oxygenated. When the singled celled prokaryotes ruled the planet there was little or no atmospheric oxygen (Butcher et al., 1992; Collerson & Kamber, 1999; Knoll, 1991, 1992; Schopf, 1992) and probably no sex (Bitter 1991; Lovelock, 1991; Margulis, 1970; Swimme & Berry, 1991). Rather, these cells would probably divide and produce two identical copies of themselves and their DNA. However, due to biologically engineered alterations in the Earth's atmosphere, climate, and so on (Joseph, 1997), and as the environment acts on gene selection, new species began to emerge.
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Over the next billion years, as the still smoldering Earth continued to cool and internal and external radiation began to taper off, and in parallel with changes in the genetically altered seas, lands, climate and atmosphere, ground hugging, water loving, cold seeking, sun worshiping, single celled, and simple multi-celled organisms gained dominion over the planet and the sunlit bottoms of innumerable shallow seas. These creatures, however, continued to biologically engineer the planet, for whereas some microbes were producing magnetite--a mineral rich substance that creates a magnetic field--others pumped out and secreted free-oxygen as a waste product. In consequence, oxygen breathing life forms were eventually provided with an oxygen rich environment and a planet with a magnetic field and thus a magnetic shield that enabled them to thrive on the surface of the Earth without risk of instant death from cosmic rays and fast-moving electrically charged particles.
OXYGEN & SINGLE CELL DIVERSIFICATION
Initially and for almost a billion years, the Earth's atmosphere was comprised of methane, ammonia, nitorgen, and carbon dioxide with little or no free-oxygen (Butcher et al., 1992; Knoll, 1991, 1992; Schopf, 1992). Because the planet was also continually bombarded by life neutralizing ultraviolet radiation, surface living oxygen-breathing life forms probably remained underground. Although the Earth's magnetic field was constructed some 3.6 billion years ago, complex life forms dependent on oxygen had to wait until almost 2 billion years had passed before the atmosphere had altered sufficiently (e.g., Collerson & Kamber, 1999; Schopf, 1992) so as to enable them to venture upon the surface of the planet.
At least some of the first single celled life forms to take root on this planet produced oxygen (and other substances, including calcium and magnetite) as a waste product. Hence, with the proliferation of life beneath the sea and beneath the earth, and over the ensuing billion years, a magnetic field was established and the atmosphere was flooded by increasing amounts of oxygen (Butcher et al., 1992; Collerson & Kamber, 1999; Knoll, 1991, 1992; Schopf, 1992; Shore 1994; Swimme & Berry 1991). These were very fortitous events, at least insofar as evolution is concerned, for not only does the magnetic field shield the planet from cosmic rays and fast-moving electrically charged particles emitted from the sun, but when oxygen is exposed to the sun's radiation, photochemical reactions occur creating a triatomic form of oxygen called ozone--which had been established by 2 billion years B.P. (Collerson & Kamber, 1999). Ozone acts as remarkable filter through which the rays of the sun must pass and which eliminates ultra violent rays.
Over the ensuing hundreds of millions of years the layer of ozone increased such that the life neutralizing effects of ultraviolet solar radiation were filtered out. Coupled wit the biologically constructed magnetic field, this allowed life to emerge from the sea and from beneath the earth and from within stone and rock, so as to diversify and evolve. Those which could breath oxygen and produced carbon dioxide as a waste product and those which were dependent on carbon dioxide but which produced oxygen as a waste product, prospered, evolved, diversified, and became increasingly interdependent. Carbon dioxide breathing plants and oxygen dependent animals soon came to rule and overrun the planet.
EUKARYOTES, MICROTUBLES & MITOCHONDRIA
The first single celled oxygen-breathing eukaryote ("true seeds") Earthlings likely emerged over 3 billion years ago (eg. Woese et al., 1990). Presumably they survived only in those sheltered biological pockets where oxygen was being actively released as a microbial waste product. By 2 billion years B.P., oxygen levels had increased sufficiently that a globalized ozone layer had been established (Collerson & Kamber, 1999). Complex oxygen-breathing life forms, therefore were able to emerge and live on the surface of the land and upon the sea. As oxygen is a superior energy source as compared to nitrates, sodium, ammonia, etc., once oxygen levels had increased sufficiently (and as the environment acts on gene selection) oxygen-breathing creatures were provided the opportunity to diversify and to "evolve" into even more complex creatures, including those equipped with the first rudimentary sensory-motor cells--harbingers to what would become neurons.
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Once these oxygen-breathing creatures emerged from their sheltered pockets they also became susceptible to invasion by yet other organisms such as mitochondria and perhaps microtubles, such that by 1.8 billion years B.P., enlarged mult-cellular life forms (e.g., acritarchs) were now contained mitochondria-like organelles (Gregory et al., 1998). As it turns out, invasion by mitochondria (and perhaps microtubles) were most fortuitous events. Once these invaders had been incorporated and symbiotic relationships were established, the rate of evolutionary metamorphosis speeded up considerably as did the rate of environmental engineering.
Mitochondria are single celled organisms which dwell within eukaryote cells (Cann et al. 1987; Yang et al., 1985). Mitochondria are considered the "powerhouse" of the cell. All nucleated, multi-cellular creatures appear to contain mitochondria within the majority of their cells (except blood cells); a relationship which in some ways parallels that of viral symbiosis. In fact, like viruses, mitochondria have their own semi-independent stores of DNA, which interact with and dependent upon the host cell's genome in order to duplicate (Cann et al. 1987). Mitochondria are not viral elements, however, but appear to be derived from alpha-proteobacteria (Yang et al., 1985) and directly related to an obligate intracellular parasite, Rickettsia prowazekii (Andersson et al., 1998). Nevertheless, like viruses, but unlike bacteria, mitochondria are incapable (at least on this planet) of living an independent existence outside a eukaryote cell (Cann et al. 1987; Yang et al., 1985).
In contrast to the destructive relationship of viruses, mitochondria provide the cell with the metabolic energy that enables it, and its DNA to function. The services provided are so important that the cell would die if deprived of its mitochondria. This suggests that multi-cellular organisms were subject to mitochondria invasion early in their history--perhaps before they became multi-cellular and perhaps inducing multi-cellular metamorphosis. This invasion (or engulfment) enabled single celled eukaryotes to become multi-cellular organisms.
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Specifically, mitochondria (and their 37 (human) genes) are located within the complex cellular cytoplasm of the cell. Most cells consist of an incredibly complex maze of spaghetti-like inner membranes which form strands of endoplasmic reticulum. Located throughout the cytoplasm, almost encapsulated by these strands of reticulum, are plasmids (free DNA), as well as Golgi bodies, and the mitochondria-- each with their own semi-independent stores of DNA.
As noted, animal cells contain thousands of mitochondria. Mitochondria come in various sizes but are also capable of growing larger or smaller, changing shape, and engaging in movement which enables them to approach one another and fuse, forming bigger structures, or cleaving in order to become shorter in size (Cann et al. 1987).
Each mitochondria contains a double membraine, which is folded together thereby forming inner, parallel plates. Within the inner folds are found cristae which manufacture and contain the enzymes responsible for converting the potential energy bound in food, into real energy (ATP) that can be employed for all cellular activities (Cann et al. 1987; Yang et al., 1985).
Specifically, mitochondria metabolize fatty acids and carbohydrates, forming water and carbon dioxide, and utilizes oxygen to fuel these activities, releasing energy rich phosphate compounds, ATP, in the process. Mitochondria act as the source of ATP production in all aerobic eukaryotic cells.
Because they act as the powerhouse of the cell, the development of this symbiotic relationship provided eukaryote cells with the capability of engaging in complex energy consuming behaviors. Moreover, because these mitochondria apparently donated much of their own intronic genes and genome to the genome of those cells they invaded, they not only magnified and increased the amount of genetic information available, but may have promoted the process of evolutionary metamorphosis by providing appropriate candidates with the genetic information which enabled them to take advantage of the planet's changing atmospheric and climatic conditions and to "evolve" into more complex creatures. For example, mitochondria DNA has a high percentage of coding (exons) DNA but are generally lacking non-coding (introns) DNA and repeated DNA sequences (Cann et al. 1987; Yang et al., 1985). This suggests that they may have donated their introns and intronic base pair sequences (and thus the genetic potential and memories they contain) to the host cell they invaded (for related discussion see Andersson et al., 1998).
The symbiotic relationship between mitochondria and eukaryotes appears to have been established by 2 billion years B.P., once the planet had become sufficiently oxygenated and covered with a protective ozone layers. Being provided with additional energy sources thus enabled evolving life to engage in complex high energy behaviors, including those involving neural transmission. However, prior to evolving neurons required an additional invasion; that is, by microtubles.
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In addition to mitochondria multi-cellular organisms are comprised of multiple microscopic organisms including microtubles (Hyams & Lloyd, 1994; Strauss & Wilson 1990). The single celled creatures that first populated this planet (bacteria and blue-green algae) were presumably without microtubules. However, some time during the last several billion years single and multi-cellular celled eukaryotes may have been invaded by microtubules, and formed a mutually beneficial relationship that was maintained symbiotically. Indeed, microtubles are an almost ubiquitous component of the eukaryote cytoskeleton, forming the structural core of cilia, flagella, playing major roles in intracellular transport and neural transmission and probably constitute more than 10% of total brain protein (Hyams & Lloyd, 1994).
Microtubules are essentially hollow cylindrical tubes, about 25nm in diamater and which are organized in tiny bundles that may run the length of the cell, and most cells contain hundreds if not thousands of microtubles (Strauss & Wilson 1990). Moreover, microtubules are alive and may have at one time contained their own DNA. Not only are they nucleated (which suggests that at one time they maintained their own genome) but microtubles behave like tiny organisms which interact with their external cellular environment and are able to position themselves and shift positions so as to move about within the cell; a consequence of changes in electric polarization which induces movement. Microtubule organisms are therefore able to approach one another, position themselves, interact, exchange material, and then separate (Strauss & Wilson 1990); just like single celled microbes. However, they do not contain an independent genome and are generated by multiple genes and gene families which are differentially expressed depending on the type and development of the cell (Hyams & Lloyd, 1994).
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Microtubles are particularly abundant within neurons and glia, with different types and shapes of microtubles located in dendrites, axons and the soma of the neuron. Microtubles in fact, span the entire length of the axon. Microtubules are responsible for both anterograde and retrograde transport of various molecules along the lengths of the dendrites and axons and play a significant role in organizing cytoplasmic polarity. They also assist in the transport of neurotransmitter substances which come to be released (by axons) and taken up (by dendrites) at the synaptic cleft. These chemical messengers enable different cells to communicate and exchange information.
Once released into the synapse, chemical neurotransmitters are absorbed by a dendrite, and via dendritic microtubules, these chemicals are transported toward the cell body within which is found the cell's DNA, at which point the dendritic microtuble interacts with the microtubles within the soma which then interacts with the microtubles of the axons. Hence, it is through the assistance of microtubules that nerve cells (and their DNA) are able to communicate and exchange information.
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Likewise, it is through the help of microtubules that single celled and multicellular creatures (who lack neurons) are able to communicate and analyze environmental stimuli (Bitter 1991; Strauss & Wilson 1990). In addition, microtubules play a role in cell division, and in this regard, they appear to have contributed to the development of sexual behavior and the evolutionary metamorphosis of complex multicellular creatures.
There are several general explanations for microtubles and their presence within multi-cellular organisms. For example, they may well be astro-biological in origin and were cast upon the face of this planet several billions years ago and subsequently invaded or were engulfed by single or multi-cellular organisms. Once engulfed they donated their DNA to the genome of the host cell whose genetic machinery now acts to reproduce them within the cell.
Another possibility is that the DNA of those single cellular creatures who were among the first to take root on this planet already contained the genetic instructions for microtuble creation. Hence, once the environment had been sufficiently altered so as to make their presence adaptive, and as the environment acts on gene selection, the DNA of single- and multi-celled creatures began to manufacture these entities, which is why most multi-cellular creatures come equipped with microtubles.
A third explanation is that microtubles evolved independently and were later engulfed. However, there is no evidence that microtubles had ever lived an independent existence on the surface of this planet, though there is evidence that microtubles may have lived independently on Mars. Indeed, the Martian meteorite examined by NASA scientists was found to contain the fossilized impressions of microtubular organisms (e.g. McKay et al. 1996). Hence, it could be argued that debris containing microtubles from Mars or some other planet, crash landed on Earth, and were engulfed and/or invaded multi-cellular organisms thereby forming a symbiotic relationship. If that is indeed the case, this proved to be a most fortuitous evolutionary development, for microtubules play a role in DNA replication and the "evolution" of increasingly complex creatures.
SEX, MICROTUBULES AND "EVOLUTION"
Some types of bacteria mate, and thus engage in "sexual" relations, so it is entirely possible that a rudimentary form of sexual behavior may have been practiced by at least some species over 3 billion years ago. However it was probably not until around one to two billion years ago that sex became a widespread form of reproduction which was likely practiced by oxygen breathing multicellular creatures who in turn became capable of indulging in more complex modes of communication.
In some respects, the same cellular susceptibility that enabled microtubles and mitochondria to invade, take up residence, and possibly donate DNA, also made it possible for other organisms and cellular life forms to invade, including Golgi bodies, as well as DNA-encapsulated sperm. Just as mitochondria, Golgi bodies, and possibly microtubles long ago donated their DNA to the genome of the host cell, where it was then incorporated (e.g. Andersson, et al., 1998), the DNA of the sperm is also incorporated. However, one incorporated sperm induces the single cell of the ovum to divide sexually, thereby creating a multicellular creature. In fact, when microtubles invaded and were incorporated, they too may have induced their single celled host to divide and become multicellular creatures.
Be it worm or human, the tissues of the body, perhaps like our ancestral multicellular cousins, are derived from a single cell; i.e. the sexually fertilized ovum. Essentially, the female ovum comes to be invaded by a spermatozoon. The spermatozoon in turn immediately loses its tail whereas its head rapidly increases in size and then disapears as it aborbs ovum protoplasm. As a consequence of this invasion the single celled ovum quickly undergoes meiosis and divides; a process which is repeated by all its daughter cells thus creating a complex multicellular organism. However, this process is also dependent on DNA and microtubular activity.
For example, the centrosome of the cell is connected to separate strands of DNA, via the microtubules. During the first stage of sexual cell division (i.e. meiosis) these DNA strands separate and chunks of chromosome become detached and are swapped with their counterparts via the assistance of these microtubles. They are then paired together so as to make new chromosomes that are arranged in combinations different from those of the parent organisms. Hence, a tremendous variety of chromosomal combinations can be produced which in turn leads to variability.
The single celled creatures that first populated this planet (bacteria and blue-green algae) were presumably without microtubules. However, perhaps two billion years ago when oxygen levels has increased sufficiently so as to generate ozone (Collerson & Kamber, 1999) single celled creatures may have been invaded by microtubules as well as mitochondria; a relationship that was maintained symbiotically. However, once this relationship was established, and sexual reproduction and chromosomal shuffling became the norm, all manner of novel life forms could be generated due to shifts in chormosomal and DNA organization and the intronic birth of genes within genes (see chapters 3,4).
Moreover, given the role of microtubules in cellular communication and active transport within neurons, once incorporated and over the course of evolution, cellular development and communication was given tremendous developmental impetus. Indeed, in addition to oxygenation and the development of sex, it may well have been advances in communication secondary to microtubular (as well as mitochondria and Golgi body) symbiosis, that gave rise not only to multi-cellular creatures but to the eventual evolutionary metamorphosis of the neuron and thus the human brain.
THE NEURONAL KINGDOM OF LIFE
It has also been estimated the single celled eukaryotes may have first emerged on Earth over 3 billion years ago (Woese et al., 1990). Since single celled creatures, such as amoeba and paramecium, are able to sense and learn from their environment, and are capable of navigating around obstacles, searching out food, and avoiding danger (Bitter 1991; Clayton, 1979; McConnell et al. 1959, 1961), it may well be the case that over 3 billion years ago single celled eukaryotes were able to behave likewise. However, since the planet had not become sufficiently oxygenated until 2 billion years ago (and at very low levels at that), it is more likely that eukaryotes did not acquire this capacity until this latter date, and only after they had been invaded (or engulfed) mitochondria and microtubles. In fact there is no evidence of symbiotic relationships having been formed until around 1.8 billion years B.P., when enlarged organic-cystic coated mult-cellular life forms, acritarchs, had emerged. Acritarchs appear to have contained mitochondria-like organelles, as well as a nucleus.
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Once microtubles and mitochondria had established residence within certain multi-cellular organisms, the ability to communicate and engage in sensory-motor behavior was given tremendous impetus, in part due to the tremendous energy being supplied (Andersson et al., 1998). Moreover, with the acquisition of microtubles organisms now had the capability to employ cells specifically for communicative purposes, thus leading to the metamorphosis of the first neurons.
Nevertheless, it appears that it was not until another 500 million years had passed before at least some eukaryotes would acquire neurons; i.e. around 1.3 billion years ago for it was during this time period that the multi-cellular ancestors for invertebrates had become established (Wary et al., 1996). These included long sinuous worms which were burrowing beneath the wet sands and in the shallow seas (Seilacher, et al. 1998). These creatures likely possessed primitive sensory-motor neurons which induced coordinated movement for the burrows of these worms show obvious signs of branching which indicate purposeful searching movements (Seilacher, et al. 1998). Presumably these sensory-motor cells were externally located outside the body, and were especially responsive to light and chemical and pheromonal messages which when activated would induce searching movements. Hence, it is possible that these particular worms may have already evolved a very primitive nerve net.
Presumably, eukaryotic life remained rather simple in organization until around 580 million B.P., when a diverse range of life forms emerged: the calcium secreting Ediacaran fauna (first discovered by R. C. Sprigg in the 1940's). Ediacaran fossils have been discovered world wide and include soft bodied, leaf- and disk-shaped, plant-like creatures, which ranged in size from over 3.5 feet to less than 1/2 inch (Glaessner, et al. 1986). However, they consisted of only 11 or fewer cell types (compared with over 200 cell types for mammals). Nevertheless, given the huge size of some of these creatures, and as some were also capable of movement, then at least some of these organisms must have also been equipped with sensory-motor neurons, as well as generalized sensory cells, and thus nervous-like tissue including a nerve net.
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Perhaps several million years after what appears to have been a mass extinction of the Ediacaran fauna (their skeletal/shell building calcium secreting mission accomplished), there ensued an explosion of life with all manner of complex creatures appearing in every river, ocean, and stream. These included organisms with a hard tube-like outer-skeleton consisting of calcium carbonate, and all manner of "small shelly fish" (Anabrites, Protohertzina), as well as sponges and jelly fish, and later, mollusks, brachipods, and the first anthropods (e.g. trilobites) which immediately sprouted legs. In fact, with no history of derivative ancestral forms, and over the course of just a few million years, all manner of complex life forms emerged, and many species were equipped with gills, intestines, joints, and modern eyes with retinas and fully modern optic lenses. In fact, every phylum in existence today (including several which have since become extinct), emerged during the Cambrian Explosion, including the phylum Chordata.
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However, not every phylum emerged simultaneously. Rather, the Cambrian Explosion was rather prolonged, with simple creatures "evolving" in advance of those which were physically, biologically, structurally, and neurologically more complex. For example, at the onset of the Cambrian explosion some organisms appear to have been equipped with nervous-like tissue e.g., sponges, jelly fish, sea anemones, whereas others may have possessed neurons strung together in the form of a nerve net, i.e., hydrozoa.
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For example, sponges (which are a step below coelenterates; e.g., jelly fish, sea anemones, and Hydrozoa), although without true neurons (Ariens Kappers, 1929; Bishop, 1956; Burnett & Diehl, 1966, Emson, 1966; Lentz, 1968; Papez 1967; Jacobson 1963), contain a very primitive organization of nervous-like tissue. This includes generalized sensory cells, the bulk of which are concentrated within and around their external orifices and pore sphincters through which sea water freely circulates. They also contain very generalized motor cells which is why young sponges are capable of amoeboid movements. It is these sensory and motor cells which presumably enable adult sponges to (very slowly) react to stimulation.
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Sponges are also capable of a very slow protoplasmic form of information transmission which is made possible via microtubular neuroid activity. In addition to microtubules, sponges contain a number of neorotransmitters such as serotonin, norepinephrine, epinephrine and acetylcholinesterase (Lentz 1968). These chemical transmitters are found in high concentrations within the human brain and are involved in memory, emotion, and movement. Hence, the nervous system of the sponge employs these neurotransmitters and displays a primitive type of neuroid transmission from which true nervous conduction may have evolved.
THE NERVE NET
Along with the sponge, hydra may have also emerged at the outset of the Cambrian Explosion; or they may well have evolved over 1 billion years ago from the ancestral burrowing worms noted above. Although we can only speculate as to the neural organization of the burrowing worms from 1.3 billion years B.P., hydra are in possession of a "true" central nervous system including a well developed nerve net (Ariens Kappers, 1929; Colbert, 1980; Jarvik, 1980; Jerison, 1973; Papez, 1967; Romer, 1970). Hence, by the onset of the Cambrian Explosion it can be assumed that the nerve net had become well established in at least some species.
The establishment of the nerve net was a major evolutionary accomplishment. With these network of interlinked neurons a multicellular organism could behave as a complete unit, in a controlled, highly coordinated and directed manner as different regions of the body could now communicate together almost simultaneously.
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Again, although a rudimentary "nerve net" may have "evolved" well over a billion years ago, it is evident that by 550 million years ago a complex network of neurons, that is a "nervous system" had been established; a development that may have coincided with the appearance of the planaria, hydra, and flat worms; i.e. the coelenterates.
Coelcenterates are the most primitive members of the animal kingdom to possess not just neurons, but a "nervous system," composed of distinct olfactory-chemical, photosensory, and sensory-motor neurons, including those which are unipolar, bipolar, and multipolar (Ariens Kappers, 1929; Papez, 1967; Lentz 1958). They also contain a third type of cell called a ganglion cell (or protoneuron). These nerve cells also possess true synapses which resemble those of the mammalian nervous system. For examle, hydra (e.g., flatworms) are symmetrical and have an enlarged anterior region which correspond to its head, and are capable of twsting, bending, swaying, and waving their tentacles which respond to a variety of stimuli. The hydra's sensory cells are located along the body surface or upon its tentacles, and which send axonal processes to ganglion cells. When food comes into contact with the surface of the mouth, sensory cells are stimulated which act on motor cells and the mouth closes and the upper body contracts which forces the food into the body cavity. In many respects the hydra could almost be characterized as a floating stomach for once the food has been taken in, the creature twists and turns and contracts in various directions. Later it will undergo a violent contraction causing undigested material to be expelled through the mouth.
However, these creatures are without true brains. Rather, in addition to the nerve net they possess a dual pair of nerve cords which run lengthways within the body--the forerunner to the spinal cord and the phylum chordata. They also possess tiny neural ganglia located in the anterior head region. These nerve cords and ganglia in turn are connected to chemosensory neurons located externally in ciliated pits within the head area and along the body surface. Specifically, some nerve cords are connected to photosensitive retinal cells found within their cephalic eyes, and others to motor and tactual-sensory neurons located on the body surface.
If we accept the modern day hydra as a representative of those worms that emerged early in the Cambrian Explosion, and as a model for nervous system development, then it would appear that sensory neurons and their dendrites were originally situated within the outer epidermis, and that motor-effector neurons were first established within the contractile motor tissue. These somewhat separate origins also suggests that a chemical, photosensitive, and motor nervous system were semi-independently evolving. That is, the brainstem may have separately evolved from collections of sensory-motor cells, whereas the forebrain may have evolved from chemically-sensitive cells, whereas the midbrain and diencephalon may have evolved form photosensitive cells. However, these different brain areas were also exchanging information as well.
Over the course of evolutionary metamorphosis and the ensuing eons of time, these original externally located sensory and motor neurons began to migrate inward and to eventually collect together within the body so as to form collections of nuclei; i.e, neural ganglia (Ariens Kappers, 1929; Papez, 1967; Lentz 1958). Likewise, what had been a simple network of neurons located beneath the skin, became ganglionic and concentrated in the anterior "head region" of many organisms, such that separate masses of ganglions were now linked together. In consequence, as the Cambrian Explosion continued, creatures such as anthropods and chordates developed true brains.
THE CAMBRIAN EXPLOSION AND THE PHYLUM CHORDATA
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The initial olfactory, visual, motor neuronal network first developed by the coelenterates was repeated and elaborated over the ensuing 50 million years of the Cambrian Explosion. However, with the evolution of anthropoids and chordates, two divergent patterns of central nervous system organization ensued. Among chordates, in addition to the head ganglions, the posterior nervous system would become stretched out, thus forming a single hollow tube that runs the length of the dorsal surface. By contrast, the central nervous system of the anthropods consists of a pair of nerve cords which run the length of the ventral surface, the belly. It if from anthropods that spiders, insects, crabs, lobsters, and shrimps evolved. However, if you turn an anthropod upside down, these nerve cords then become dorsally located, similar to vertebrates.
Those creatures whose decendants were destined to become vertebrates increasingly adapted to a life of swimming and they evolved an internal skeleton of rigid bone and cartilage which forms internally by accretion. By contrast, anthropods shed and then replace the external skeleton.
Like those who had come before them, these primitive and ancient pre-vertebrate animals maintained specialized neuroganglia sensitive to tactile, visual, and chemical/pheromonal (olfactory) stimulation, as well as ganglia involved in tactile-motor functions. As such, the first rudimentary features of what would become the olfactory-amygdala-straital forebrain, the visual midbrain, and the sensory-motor brainstem were probably first established almost 500 million years ago, during the latter phases of the Cambrian Explosion. Indeed, it was during this time period that the representative of the phylum Chordata emerged. These included tunicates (subphylum Urochordata) and the first jawless fish (e.g. Astraspis, Arandaspis) who possessed a notochord and an elongated brain that consisted of a spinal cord, brainstem, limbic forebrain. Hence, by time the first vertebrates and armored fish begin to swim the oceans, around 500 million years ago, the forebrain and brainstem and thus the brain had become fashioned (Ariens Kappers, 1929; Colbert, 1980; Jarvik, 1980; Jerison, 1973; Joseph, 1993; Papez, 1967; Romer, 1970), thereby giving rise to a cerebral and thus a cognitive explosion.
THE BRAINSTEM & MIDBRAIN
By 500 million years ago, motor nerve neural networks and related neural ganglia became increasingly organized and collected together thereby giving rise to the brainstem in species such as jawless tunicates and amphixious (protochordates) -the ancestors to true vertebrates.
The ancient brainstem (which soon differentiated into a medulla and pons) was (and continues to be) concerned with monitoring and controlling heart rate, breathing patterns, cortical arousal, sensory filtering, and reflexively triggering specific motor reactions to visual, vestibular, painful, sexual, and edible stimuli (Blessing, 1997; Donkelaar, 1990; Vertes, 1990). Over the course of evolution, the brainstem continued to evolve and contributed to the development of the posterior-ventral portion of the midbrain (see Romer, 1970; Sarnat & Netsky, 1974). Indeed, the caudal midbrain is tightly linked and in many respects anatomically resembles the brainstem. And spanning the length of both structures are reticular neurons.
Whereas the brainstem may have been fashioned from collections of sensory-motor neurons, the anterior-dorsal midbrain (and dorsal thalamus; Butler 1994) appears to have had a different origin. As noted, billions of years before the Cambrian Explosion, single celled organisms were engaging in photosynthesis and likely possessed photosensitive cells, even though they lacked eyes. Initially these cells were more concerned with extracting photo-chemicals from light and later evolved the capacity to detect various shades of illumination. However, as the DNA of these cells also contained the genetic potential for generating the capacity to see, and as the environment acts on gene selection, once the ozone layer had been established and the atmosphere to clear and to be saturated with oxygen, innumerable species emerged from their sheltered pockets and thus developed the capacity to distinguish light and shadow and form and shape. That is, the oxygenation of the planet including oxygenation of the oceans, contributed to the ability to develop vision.
These initial photosensitive cells were probably dorsally located. It is these photosensitive cells which would later give rise to the retina and yet others which would migrate internally to form visually sensitive neural ganglia. This light sensitive neural ganglia soon became the visual midbrain, dorsal thalamus, epithalamus, and dorsal hypothalamus; nuclei which over the course of evolution would serve as a bridge linking the motor-sensory brainstem/spinal cord with the chemically and olfactory sensitive forebrain-telencephalon.
However, within the forebrain, dorsal and caudally located neural tissues immediately adjacent to the diencephalon/brainstem, also became sensitive to visual information; i.e. the hippocampal portion of the amygdala-striatum. As will be detailed below, the forebrain initially consisted of a relatively undifferentiated collection of neural tissue, a composite of what would later (around 300 million years B.P.) become the amygdala, striatum, and later, the hippocampus. Specifically, because the hippocampal portion of the amygdala-striatum could detect light and shadow, this composite forebrain structure also evolved the capacity to direct the brainstem motor centers so as to approach (or avoid) light vs darkness, and gained the capacity to retain this information, thus forming visual-motor-spatial memories which assisted the organism when navigating and moving about their environment. That is, the hippocampus evolved "place cells."
As noted, some of those life forms which were among the first to take root on this planet digested minerals, inorganic substances, organic molecules, or relied on sunlight and photosynthesis as sources of energy. Those which were digesting organic and inorganic substances, therefore, possessed the capacity to manufacture the necessary chemical and enzymes which would be secreted in order to act on and break down these substances. These DNA-based capacities were thus harbingers to what would become the capacity to manufacture neurotransmitters.
As simple then complex multi-cellular creatures evolved, these DNA-chemical manufacturing capacities also evolved. Initially, these chemically secreting cells were externally located, whereas over the course of evolution, some of these cells migrated internally, forming chemically secreting ganglia, some of which eventually coalesced within the brainstem, whereas yet other became situated in the forebrain as an extension of chemically sensitive cells that remained externally located, thus giving rise to what would become the olfactory system. However, as noted, possibly even before the establishment of the nerve net, animals such as the sponge had presumably evolved the capacity to manufacture neurotransmitters well over 500 million years B.P.
THE OLFACTORY-AMYGDALO-STRIATAL-HIPPOCAMPAL FOREBRAIN
For the first several billion years after the Earth was formed, chemically sensitive cells were originally located externally, some of which later became localized around a food consuming orifice. Be it a single celled chemoautotroph, or multi-cellular eukaryote, via the analysis of chemical secretions, a potential edible substance might be detected at a distance, could be deemed good to eat and was approached and consumed. Over the course of evolution, and since it is not very adaptive merely to absorb, or eat whatever comes into one's mouth, the ability to make distinctions, to recognize, and to make comparisons was also necessitated which resulted in the creation of memory -and this too was accomplished through chemical analysis and smell, and then later, via taste.
Over the course of "evolution" some of these chemically sensitive cells migrated internally, such that, during the course of the Cambrian Explosion, some became situated within the mouth and the "nose" thereby forming a specific collection of olfactory and pheromonally sensitive ganglia, which in turn would become the olfactory bulb and then the olfactory lobe and thus the limbic forebrain which initially was a somewhat undifferentiated composite of amgydala, striatal, and hippocampal tissue (the amgydalo-striatal gray).
As olfactory molecules could signal the presence of food, or a predator, or a sex partner, or a competitor, the olfactory bulb and olfactory lobe, and thus the olfactory-limbic system including the amygdala portion of the amygdala-striatum initially became concerned almost exclusively with feeding, fornicating, fighting, or fleeing (Joseph, 1992a, 1994, 1998a). As these chemicals were often secreted and detected at a distance, however, the olfactory forebrain was also provided a "pregnant interval" (Herrick, 1925) before it need respond. Because it need not respond immediately, it could also keep this information "in mind" thus giving rise to short term memory. Coupled with its ability to form long term memories so as to make distinctions and comparisons, the forebrain also became a memory center that was also storing in memory visual-spatial information as received by the hippocampus. Finally, because ultimately this information would often necessitate movement, the striatal portion of the forebrain became increasingly concerned with coordinating gross movements in response to directives from the hippocampus and the amygdala. Initially, however, that is during the later portion of the Cambrian Explosion, the amygdala-striatal-hippocampus formed a composite structure, i.e. striatoamygdaloid gray (limbic forebrain), which was essentially an extension predominantly of the olfactory system (Gloor, 1997; Stephan, 1983).
The limbic forebrain therefore, evolved predominantly from the olfactory system (Gloor, 1997; Herrick, 1925; Nieuwenhuys & Meek, 1990ab), and thus has an origin which is somewhat (but not completely) distinct from the midbrain, brainstem, and spinal cord. Indeed, with the exception of the visually responsive hippocampus, the limbic forebrain has an "olfactory" neural organization. In fact, this pattern of olfactory "neural" organization beginning with tunicates and cartilaginous fish, has not only been retained in all subsequent animal species, but it provided the foundation for what would become the telencephalon and the neocortex (e.g. Allman, 1990; Haberly, 1990).
Hence, to recapitulate, in contrast to the brainstem which reflexively reacts to proximal stimulation, the olfactory forebrain is able to sense stimuli at a distance, and thus has time to react. Because it need not react immediately, and as there are numerous chemicals within the external environment, the olfactory forebrain also evolved the capacity to selectively attend to and retain specific information. The olfactory forebrain thus became capable of learning and remembering. Memory, is thus olfactory in origin, as is the amygdala and portions of the hippocampus, the two main memory centers of the brain.
JAWLESS, & CARTILAGINOUS FISH
With the evolutionary metamorphosis of jawless and cartilaginous fish (Cylcostomes), the basic organization plan for the spinal cord, brainstem, midbrain, and olfactory forebrain had come to be established. In addition, the diencephalon had emerged, linking the forebrain with the brainstem, the ventral hypothalamic portion acting to notify the anterior and posterior halves of the brain regarding the internal status of the organism, and the dorsal thalamic portion becoming a major processing and relay center, transferring sensory signals to the forebrain.
Although more ventrally situated, the hypothalamus consists of dorsal and ventral as well as anterior, lateral, medial, and caudal subnuclei. Although it is true that the more ancient aspects have been well conserved over the course of "evolution" the human hypothalmus is much more complex than that of a fish or shark as it also consists of additional nuclei which perform functions associated with sexual posturing, pregnancy, lactation, and menstruation.
Nevertheless, like the dorsal thalamus, the hypothalamus may have first emerged well over half a billion years ago, and was probably exceedingly responsive to light vs darkness, including visual signals transmitted from photosensitive cells located in the anterior head region. Although the mammalian hypothalamus no longer receives input from the third eye, like the lateral geniculate nucleus of the thalamus, it receives direct retinal input via retinal axons. Hence, certain subnuclei have remained exceedingly responsive to light vs darkness.
Because large portions of the anterior-dorsal midbrain, dorsal thalamus and dorsal hypothalamus were initially derived from photosensitive cells and because these cells are effected by the rhythmical nature of the planet's rotation (which induce rhythmical periods of light and dark), photosensitive neurons located in these tissues also became adapted to these alterations and thus rhythmically sensitive (see Aronson et al. 1993; Morin 1994, for related discussion). Eventually they became capable of inducing and enforcing rhythmic activities within the central nervous system, including the forebrain, via their control over arousal and the production of norepineprine, serotonin, and dopamine --neurotransmitters which are manufactured by neurons located near the midbrain-brainstem junction (chapter 17). In addition, the manufacture and release of these neurotransmitters is also rhythmical, which in turn effects the overall functioning and arousal of the brain.
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With the transition from tunicates to cartilaginous fish and the evolution of primitive jawless fish, 500 to 450 million years ago, the brainstem sprouted a number of cranial nerves through which it received and transmitted inpulses especially those related to the vestibular system. Moreover, with the evolution of gills and the tongue, the brachial nerves evolved which in turn were initially concerned with controlling the gills and movement of the tongue (Romer, 1970). The tongue may well have been the first muscular appendage subject to fine motor control, and it is a structure which first appears in Cyclostomes. Like the brainstem and forebrain, however, the tongue became more fully developed with the evolution of amphibians (i.e. frogs) and reptiles and snakes (Colbert, 1980; Jarvik, 1980; Jerison, 1973; Romer, 1970).
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With the evolution of the jaw, and thus the first jawed armored fish, around 450 million years ago (Caroll, 1988; Colbert, 1980; Jarvik, 1980; Romer, 1970) the brainstem underwent even further elaboration so as to coordinate the movements of not just the tongue but the mouth.
Initially there were at least two types of jawed species, one line of which diverged and gave rise to cartilaginous sharks and rays (elsmobranchs) -creatures which first appeared about 400 million years ago (Caroll, 1988). Sharks possess a well developed brainstem, olfactory limbic forebrain, and a large optic lobe (or tectum/colliculus) situated atop the midbrain (Haberly, 1990; Smeets, 1990).
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Midbrain Optic/Auditory Tectum.
With the further evolution of sharks and other jawed creatures, the inferior portion of the midbrain optic tectum eventually became reorganized and increasingly concerned with processing and orienting toward auditory-vibratory stimuli. Over the course of evolution, the inferior portion of the midbrain gave rise to the inferior colliculus which is concerned with analyzing and responding to auditory stimuli by triggering head and body movements toward the source. In sharks auditory-vibratory information is received via receptors located in maculae sacculi (Smeets, 1990), whereas machanical and electrical inpulses are received via the lateral line system -all of which are then relayed to the brainstem and cerebellum, and then the midbrain and telencephalon via the thalamus. [-INSERT FIGURES 20 & 21 ABOUT HERE-]
The cerebellum first evolved over 450 million years, well before the emergence of the first vertebrates, and is thus a characteristic part of the brain in cartilaginous fish and prevertebrates, as well as in fish, amphibians, reptiles, birds, and mammals (Larsell, 1967-1972). Specifically, the cerebellum evolved out of the vestibular nuclei and is derived from the rhombic lip and ectodermal thickenings around the cephalic borders of the fourth ventricle. The cerebellum, however, began as a rudimentary appendage to the brainstem, as is evident in hagfish and lampreys, and then progressively increases in size in the progression from fish to mammals.
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Hence, during the early stages of evolution, as primitive creatures were without limbs, they possessed only a small nubbin of cerebellum - referred to as the flocculonodular lobe -what would become the paleocerebellum (also referred to as the archicerebellum). This tissue presumably acted to coordinate the axial muscles which the position of the head, trunk, and eyes, and probably also acted to integrate these movements in response to motivational commands transmitted by the limbic system.
THE EVOLUTION OF THE OLFACTORY LIMBIC FOREBRAIN
The olfactory system probably gave rise to a very primitive amygdala-striatum-hippocampus some 500 hundred millions years ago when the protochordates first emerged and the ancestors of the first eel-like cyclostomes and the wormlike, burrowing, limbless Gymnophiona first slithered upon the scene (Colbert, 1980; Jarvik, 1980; Jerison, 1973; Romer, 1970). The modern day descendants of these creatures are apparently little different from their ancestors and possess a hypothalamus, olfactory system and a amygdala-striatum-hippocampus (Ariens Kappers, 1929; Papez, 1967).
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This neural organizational and structural pattern was retained but became more elaborate over the ensuing 100 million years, as is evident from an examination of the brain of cartilaginous fish. Cartilaginous "fish" such as sharks, are considered a "living fossil" and first began to swim the seas 450 million years B.P. Dissection of the shark brain reveals a large forebrain and large olfactory bulbs (see Figure ).
The majority of the shark forebrain consists of a dorsal and ventral amygdala-striatum (also referred to as the striatoamygdaloid gray) as well as a medial-posterior hippocampal-striatum (also referred to as the medial pallium). Thus the amygdala and striatum are enmeshed forming a dorsal lateral/ventral lobe, and the medial posterior striatum-hippocampus are ensmeshed forming a medial core, as is also evident in cyclostromes, fish, and (to a much lesser degree) in tailed amphibians (urodela).
It is also evident, at least from an examination of ancient endocasts, that cartilaginous and armored fish, who swam the seas over 400 million years ago possessed a forebrain which, when the olfatory bulb and tracts are included, constitute well over half the entire brain (see Figure ). Thus early in the course of animal and neurological evolution, the forebrain was the dominant brain structure--at least in gross size. The forebrain, however, consisted almost entirely of a dorsal/ventral amygdala/striatum and the medial/posterior hippocampus/striatum which formed a composite allocortical structure, with the former dominated by the olfactory system and the latter dominated by the visual system (Haberly, 1990; Smeets, 1990; Ulinksi, 1990).
This composite pattern of neurological forebrain structural organization was retained even after the first lobed finned fish emerged from the waters to venture upon land. In fact, once animals began to dwell upon the surface of the odorous perfumed earth, olfactory cues assumed increased importance, such that the forebrain began to expand and land living animals evolved a vomeronasal organ and an accessory olfactory bulb and accessory olfactory tract so as to accommodate the demands of living in an olfactory world. Once they had become adapted to dry land, the expanding amygdala, striatum, and hippocampus became separate structures
BONY FISH, LOBED FINNED FISH, AND LUNG FISH
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With the evolution of jawed and bony fish about 400 million years ago (Caroll, 1988), the arches between the brachial clefts (or gills) became increasingly modified and much smaller and increasingly concerned with supporting the jaw (Romer, 1970; Sarnat & Netsky, 1974). Hence, over the course of phylogeny the brachial arches eventually became the mandible and maxilla of the jaw; events which coincided with major alterations in specific brainstem nuclei and the later development of specific cranial nerves associated with the jaw and facial musculature. For example, the brachial nerves became specialized and split off to form the vagal, glossopharyngeal trigeminal, and facial nerves (Romer, 1970; Sarnat & Netsky, 1974) whereas what would become the periaqueductal gray became to differentiate--a structure that would later become modified so as to coordinate the oral musculature for the purposes of vocalization.
At least one brach of bony fish gave rise to the sarcopterygian (lobe finned), fish who appeared during the Devonian age, some 400 million years ago (Caroll, 1988). Lobed finned fish possessed a cranium which was divided into two parts (a frontal-sphenoid portion and an occipital region). They had also evolved a brain and cerebellum that in many respects is quite similar to that of amphibians and even reptiles (Nieuwenhuys & Meek, 1990b; Stephan, 1983). Like sharks, lobed finned fish never became extinct as over 80 specimens have been caught off the coast of southeast Africa over the course of the last 50 years (Nieuwenhuys & Meek, 1990b).
With the evolution of bony fish, and then the lobe finned fish (Sarcopterygii), and lungfish (Dipnoi), the forebrain began to mushroom outward, forming a distinct telencephalon. These forebrain structures also increasingly became the recipient of visual, acoustic, and lateral line information which was relayed via the brainstem, midbrain, and thalamus (Butler 1994; Nieuwenhuys & Meek, 1990; Stephan, 1983). The subpallium (or floor) as well as the hemispheres of the telencephalon also became increasingly differentiated into distinct nuclear groups (Nieuwenhuys & Meek, 1990). For example, the amygdala-limbic (ventral) striatum, and the corpus (dorsal) striatum, ballooned outward to become the caudate, putamen, and nucleus accumbens. Also, a definite two layered cortex began to form along the pallial surface of the telencephalon (Nieuwenhuys & Meek, 1990) which in turn was likely a derivative of the midbrain. Over the course of evolution, neurons contributed by and related to the amygdala, hippocampus, and septal nuclei, would increasingly sandwich themselves between these two layers, eventually giving rise to neocortex.
In addition, among some species the brainstem became more complex and increasingly adapted for controlling breathing, which in turn coincided with the development of "lungs" --evolutionary events that were not random but under precise genetic control. Moreover, some species developed both lung and limbs, including Dipnoans and Coelacanths who began to venture forth upon the Earth. In addition to their dorsal fins the lobefinned Coelacanths possessed two well formed "fleshy-lobed" paired fins: the internal skeleton of which includes a humerus, femur, radius, ulna, tibia and fibula (Caroll, 1988; Jerison, 1973; Nieuwenhuys & Meek, 1990b; Romer, 1970). These lobe fins although acting to improve swimming and maneurability, also enabled these fish to probe and root among the fertile ocean floor and eat of its plant and other organic life (Jerison, 1973; Romer, 1970). Hence, it is from these lobed fins that legs would eventually "evolve" (Colbert, 1980; Jarvik, 1980; Jerison, 1973; Romer, 1970).
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The lobed "fleshy" finned lung fish were in fact the perfect transitional species. Indeed, numerous species of lobed-fins lived mainly in rivers and freshwater seas and could venture forth and live on land due the to internal air sacs embedded within their fins. These air sacs could pass oxygen directly into the blood stream. This "breathing" ability enabled them not only to venture forth, but to hole up in caked mud during the dry seasons.
Moreover, unlike other fish which are externally fertilized and which lay eggs in the open water (which are then greedily gobbled by yet other denizens of the sea), the lobe finned lung fish were fertilized inside the body and could bear the young alive. These events coincided with major adaptions within the hypothalamus which developed additional nuclei that subserved the hormonal events associated with "pregnancy" and live births.
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EUSTENOPTERONS, ICHTYOSTEGA & AMPHIBIANS
As the descendants of the fleshy finned lung fish became adapted to living on dry land, and as the environment acts on gene selection, the lobed fins underwent further modification due to the gravitational demands of a dry land environment. That is, the forces of gravity require strength in the supporting and moving appendanges, such that in consequence, legs evolved. Soon such creatures were able to expend a greater amount of time out of the water and began to diversify. Hence, by 350 million years ago the lobe finned fish presumably evolved into a fish with four and seven toes legs, the eusthenopteron and ichthyostegas. These amphibian-like creatures looked something like a cross between a fish and a big salamander, with flat heads and long tails, and short stocky feet like a turtle (Caroll, 1988; Colbert, 1980; Jarvik, 1980; Jerison, 1973; Romer, 1970). Presumably it is these intermediate species which in turn evolved into amphibians, some of which grew up to 15 feet length.
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It is possible that eusthenopterons, as well as the Ichthyostegas, like bony and cartilaginous fish, were equipped with a lateral line system which enabled them to perceive vibration and rudimentary sound. However, because they were also walking on dry land, they had also evolved specialized nuclei that could respond to vibrations transmitted through the feet and the legs, which were hitched directly to the skull. This enabled these and like-minded animals not only to walk but to perceive and hear vibration transmitted through their feet.
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The Evolution of Auditory Perception
Once vibrations could be transmitted directly to the skull, as the environment acts on gene selection, the brainstem underwent further modification and evolved an additional cranial nerve, in order to receive, process, and act on this information. Hence, once the descendants of the lobed finned lung fish had become fully adapted to living on land, that is around 350 to 300 million years ago, the acoustic nerve appeared as a derivative of portions of the vagal, glosopharyngeal, and facial nerves and the vestibular nuclei (Sarnat & Netsky, 1974). It is from the brainstem vestibular system that the mammalian auditory system evolved (Ariens Kappers, 1968; Papez, 1967).
However, the first amphibians and reptiles lacked an inner or true middle ear, but were capable of hearing low level vibrations and sounds, such as croaking, tails thumped on the ground, and a few distress calls and those of contentedness. Limbic language capabilities and the ability to engage in complex auditory communication is not well developed in these creatures as sound production is for the most part reflexive and mediated by upper brainstem nuclei (the periaqueductal gray). Purposeful vocal communication would first require tremendous alterations in the ability to hear sound which in turn would promote the ability to purposefully produce sound.
As noted, the development of hearing was a consequence of the evolutionary metamorphosis of the vibratory sense and the lateral line organs; structures which make their first rudimentary appearance in cyclostomes (van Bergeik, 1966). However, among bony fish, a well developed closed canal system of lateral line organs had long ago developed beneath the scales and within the skin. It is the membrane that covers these canals which responds to and transmit vibrations picked up in sea water.
However, sharks and bony fish do no perceive sound per se (van Bergeik, 1966), at least in the manner analogous to mammals. Rather, in the progression from cartilaginous to lobed finned fish, the lateral line system became increasingly modified so as to form the labyrinth which in turn was capable of detecting the animals own movements as well as that of other creatures (van Bergeik, 1966). In more advanced vertebrates the labyrinth forms and leads to the creation of the three semicircular canals which are responsible for perceiving motion, movement, and spatial orientation. Over the course of evolution, nerves from the semicircular canals in turn became enmeshed within the acoustic nerve. Together they terminate within the medulla of the brainstem and send collaterals to the evolving cerebellum and the inferior auditory midbrain tectum.
As noted, the mammalian auditory system did not evolve from the lateral line but from from the jaw and scapula and a cluster of nerve cells located within the brainstem, the vestibular nucleus (Ariens Kappers, 1968; Papez, 1967). That is, the ability to hear sound is derived from vibratory perception and which was initially made possible via bone conduction.
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Once the first amphibian-like creatures evolved and began to crawl upon dry land, some 350 million years ago, bone conduction replaced the lateral line system as a means of detecting vibrations and thus the rudiments of sound (Tumarkin, 1968). However, because these creatures at first crawled upon their bellies, they were able to detect vibrations through their legs as well as through the lower jaw which would stereotypically rest upon the ground. In consequence, the hyomandibular bone of the bony (jawed) fish evolved into the amphibian (and mammalian) stapes. In addition, the vestibuloscapular bone located atop the scapula of the amphibian shoulder became modified to form the vestibuloscapular ossicle which enabled vibrations to be perceived through the legs even when the head and jaw were no longer on the ground (Tumarkin, 1968).
With further refinements in the structure and support of the jaw, and with the evolution of reptiles, and then the repto-mammals and then the dinosaurs some 250-225 million years ago, the articular and quadrate bones (which formerly supported the mandible) became modified along with the stapes to form the three ossicles of the middle ear. What had been the amphibian vestibuloscapular ossicle, evolved into the oval window (Tumarkin, 1968). When this occurred, the dorsal midbrain (the inferior auditory tectum/colliculus) had become mammalian-like in organization and specialized for perceiving, analyzing, and orienting toward complex sounds. However, with the evolution of reptile, the midbrain underwent further elaboration, and a specific structure evolved which made the possible the ability to vocalize a range of sound; i.e. periqueductal gray. Specifically, the midbrain periqueductal gray became specialized for coordinating the oral-facial, laryngeal, and respiratory muscles which enabled reptiles, repto-mammals, and all subsequent creatures to vocalize.
Whereas initially the cerebellum received information from the lateral line organs and vestibular complex of the fish (which conveyed information regarding balance and a primitive form of hearing via vibration), as life forms took to living on dry land, the cerebellum began to progressively expand in accordance with the increased input being provided, receiving visual, proprioceptive, somesthetic, and complex auditory stimuli.
With the evolution of amphibians and true legs the cerebellum was forced to assume new roles, including the coordination of axial (trunk) and appendicular (limb) muscles which it influences via feedback from the spinocerebellar tracts.
As an evolutionary outgrowth of the vestibular system, a primary concern of the cerebellum has been and continues to be stablizing the body and acting to coordinate the axial muscles which the position of the head, trunk, and eyes.Thus as animal life began to wonder about the earth on four (and later two) legs, the anterior lobes of the cerebellum began to evolve in order to meet these demands. Thus disturbances of this region can therefore result in dystaxia predominatly in the legs. Moreover, the cerebellum began to expand in parallel with the increased size and complexity of the telencephalon--structures which would also transmit to as well as receive input from the cerebellum. It also expanded its interconnections with the limbic forebrain so as to react in accordance with affective needs. Thus the cerebellum also evolved the capacity to integrate these movements in response to motivational commands transmitted by the limbic system.
Later, with the emergence of bipedal posture increasingly complex demands were placed on the anterior and the emerging posterior cerebellum in order to coordinate gait and upper as well as lower limb movements. This corresponded with the evolution of the neocerebellum (including the dentate gyrus and the cerebellar hemispheres), which in turn paralleled neocortical expansion in the forebrain and the development of temporal sequential and fine motor functioning. In modern creatures, including humans, disequilibrium of stance and gait with little or no extremity dystaxia is usually due to lesions in the flocculonodular lobe (caudal vermis).
THE AMPHIBIAN AND REPTILIAN OLFACTORY LIMBIC FOREBRAIN
The first amphibians evolved from probably a variety of precursor forms, including the freshwater dwelling rhipidistians (a bran of the crossopterygians), some 350 to 400 million years ago, during the Devonian (Caroll, 1988). The amphibian brain, although sharing basic similarities with the brain of the fish, underwent an expansion in the dorsal amygdala-striatum such that the amygdala began to split off. Moreover, with the expansion of olfactory cortex including the development of an accessory olfactory lobe, the vomeronasal organ, the olfactory system obtained and gained a privileged access to the telencephalon and further acted to push apart the amygdala and striatum, thus creating a completely separate amygdala.
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In amphibians, it is noteworthy that the main oflactory system also terminates on the medial pallium/hippocampus. However, with the evolution of reptiles, the main olfactory system joined the vomeronasal organ (see below) and increased the size of its projections to the amygdala, and increased its representation further with the evolution of mammals. In consequence, as the hippocampus also received olfactory input, the connections between the amygdala and hippocampus underwent significant expansion and both became concerned with analyzing and remembering various aspects of the new olfactory world. In the process, the amygdala became increasingly associative, and dominated by olfactory sensations, and increasinlgy capable of mediating all aspects of olfactory-emotion. In conjunction with the hippocampus, the amygdala was also able to create an olfactory map of external reality and to related this to internal reality. However, in acquiring the capacity to differentiate between an internal and an external reality, personal identity began to emerge.
Initially, olfactory sensation provided the foundations for a personal reality, that is, through marking. What is marked indicates a personal identity and personal possession, be it territory or a sex partner. Thus, once animals had become adapted to dry land they also developed personal identities which was mediated and sustained via the olfactory limbic system, the amygdala in particular.
The Vomeronasal Organ
With the evolution of amphibians (the tailless anura) the forebrain and olfactory system expanded in response to the motoric and olfactory demands of living on dry soil including those related to the ability to perceive pheromones.
Living in a perfumed world of smell, and as the environment acts on gene selection the olfactory cortex began to expand its projections to and representation within the forebrain. In addition, an accessory olfactory lobe evolved coupled to a vomeronasal organ which was specialized for analyzing these additional and more varied and complex olfactory sensations, including those chemical messengers referred to as pheromones.
Fish, sharks, and other non-mammalian denizens of the sea, do not possess a vomeronasal organ (Smeets, 1990). Rather, these creatures have only two chemosensory systems, taste and olfaction which they employ to detect motivationally significant stimuli such as the presence of food, a mating partner, or a predator.
Hence, in contrast to fish, who use olfactory to detect distant emotionally and motivationally significant stimuli, with the evolution of the vomeronasal organ, amphibians were provided the ability to detect distant olfactory cues distinct from those of the main olfactory system, thus conferring a tremendous ability to detect and analyzed local and distant, recent and past events and stimuli including those related to the presence of predators, prey and potential sex partners. Indeed, in amphibians and reptiles, the vomeronasal organ is involved in mediating the classic four "fs" feeding, fighting, fleeing, and sexual activity, as well as promoting social behavior; i.e. aggregating (Halpern, 1987).
The vomeronasal organ projects through the amygdala in order to reach the hypothalamus which thus became increasingly specialized to process and respond to, as well as secrete chemical messages, in a reflexive fashion. The hypothalamus also began to respond to pheromonal cues by relating this information to sexual and reproductive status which it in turn could signal via the release of various hormones.
The evolution of the vomeronasal organ was a completely novel development which resulted in major alterations in the structure and organization of the forebrain. For example, in addition to the altered organization of the hypothalamus, the amygdala became a completely separate structure (Herrick, 1948; Nieuwenhuys, 1967), due to the evolution of the vomeronasal organ which transmitted directly to the amygdala. The amygdala also increased in size and evolved new functional capacities and additional subnuclei in response; i.e. the lateral and medial segments.
The Amygdala, Pheromones and Emotion
As the olfactory system more than doubled in size and importance, it increased its privileged access to the telencephalon and further acted to push apart the amygdala and striatum, thus creating a completely separate amygdala (Stephan & Andy, 1977). Through this reorganized and more emotionally-sensitive amygdala, and via the nascent vomeronasal organ and enlarged olfactory system, amphibians were provided the ability to analyze distant as well as old and recent olfactory and pheromonal cues that could not be detected by main olfactory system (MacLean, 1990).
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For example, via the detection of pheromones the organism could determine the intent and social-emotional status of conspecies who may have passed by hours or even days before, as well as signal and leave chemical messages conveying it's own intent, motivation, social position, and/or sexual availability (Ackerman 1990; Blum 1985; Mayer & Mankin 1985; Michael & Keverne, 1974; Tamaki 1985; Wilson, 1980). Moreover, not just food and potential mates, but status, aggressive vs submissive intent, sickness and health, and individual identity could be easily ascertained as well as signaled via the secretion and perception of pheromonal signals, including those that could instruct in a step-wise fashion, complex behaviors including those pertaining to sex; e.g. approach, mount, insert penis, thrust, and thrust again. In fact, just as these phermonal secretions can trigger reflexive sexual behavior in most species, direct electrical activation of these limbic structures (e.g. the amygdala, hypothalamus) can produce involuntary sexual responses including ovulation, uterine contractions, penil erection, thrusting, ejaculation and orgasm (Backman & Rossel, 1984; Currier et al., 1971; Freemon & Nevis,1969; Warneke, 1976; Remillard et al., 1983; Shealy & Peel, 1957).
With the evolution of reptiles the vomeronasal organ had also become well differentiated. The amygdala also became organized so as to process and analyze external olfactory and pheromonal stimuli and to determine its possible social, emotional, motivational, and sexual significance--a capacity that quickly came to include the ability to process visual and auditory stimuli in a likewise fashion (Gloor, 1997). That is, capacities that evolved in response to olfactory input could now be used for analyzing visual and auditory input that was being provided to the forebrain from the expanded brainstem. Moroever, the amygdala and the hippocampus began to store this information in memory, so as to make comparisons with previous impressions, and could relay these impressions to each other and to other forebrain structures for additional analysis.
The Amygdala Striatum
Because these animals were living in a world where visual and auditory input was magnified, the amygdala also began to receive visual and auditory input which was projected to it via the thalamus (Stephan, 1983). In consequence, the amygdala, therefore, was able to apply olfactory and pheromonal analytical principles to auditory and visual input, and thus scrutinize this information for motivational, sexual, and emotional significance. And, through its still extensive interconnections with the striatum, it evolved the capacity to transmit emotional signals motorically and which could thus be detected by other animals visually. Animals were evolving what would become body language and signature displays (Maclean, 1990).
The striatum, therefore also evolved new capacities due to the increased motor demands of living on dry land, such that the motor aspects of the striatum began to increasingly differentiate and to evolve in response to and in order to meet these new motoric needs. The dorsal aspect of the striatum became a rudimentary dorsal striatum, and the ventral aspect became the ventral (limbic) striatum, whereas what would become the hippocampus remained dorsal-medially located and part of the medial striatum (Gloor, 1997; Stephan, 1983); i.e. the light and visually sensitive medial pallium.
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To recapitulate, this great expansion and reorganization of the amygdala/hippocampal-striatum was initiated with the evolution of the first amphibians. The first amphibians probably evolved from a variety of precursor forms, including the freshwater dwelling rhipidistians (a branch of the crossopterygians). This was 350 to 400 million years ago, during the Devonian (Caroll, 1988). The amphibian brain shares basic similarities with the brain of the fish. However, as these and other species became adapted to living on land, the dorsal amygdala-striatum began to expand in response to increased olfactory, visual and auditory input, and in consequence the amygdala began to split off from what had been a composite amygdalostriatum (Stephan & Andy, 1977)--a consequence also of penetrating fiber pathways directed to it and the striatum by the visual and auditory systems and the enlarged olfactory system.
However, it should be noted that although the hippocampus is considered part of the limbic system and the limbic forebrain, that it does not have an olfactory neural organization (Ulinsky, 1990). Moreover, the hippocampus is exceedingly sensitive to visual stimulation, and is capable of forming and remembering a visual-spatial map of the external environment. The hippocampus is also associated with motor functioning. Indeed, memory, motor functioning and spatial mapping of the environment are in fact linked, for if one is to navigate through the environment, they need to remember why and where they are going, and how to get there--functions associated with the human and non-human hippocampus (see chapters 13, 14). Given that the hippocampus was originally dorsally located, and in "lower mammals" consists of dorsal as well as ventral aspects, and as other dorsal structures such as the dorsal midbrain and thalamus are in part derived from the visual system, then it may well be that the dorsal hippocampus is also visual in origin, whereas the ventral hippocampus is an olfactory derivative.
However, over the course of "evolution" the dorsal hippocampus has migrated to a more ventral position, fashioning the medial parietal and medial-caudal temporal lobe in the process. Hence, in the human brain, the ventral and dorsal hippocampus is instead referred to as the anterior and posterior hippocampus. In addition, there is evidence to suggest that these two aspects subserve different albeit related functions. For example, in the transition from short term to long-term memory, it appears that "memories" migrate from the anterior to posterior hippocampus (see chapter 14).
THE DIENCEPHALON: DORSAL VISUAL THALAMUS AND HYPOTHALAMUS
The Visual Thalamus and the Third Eye
The thalamus is part of the diencephalon, and serves as an interactive "bridge" that links the brainstem and forebrain, acting to relay and regulate information flow between these two structures. It was possibly around 500,000 million years ago, during the Cambrian Explosion, that the thalamus began to rapidly evolve. Due to its its dorsal superior position atop the ancestral brain, it received and was quite responsive to overhead ambient light, and apparently received visual signals through retinal neurons located in a depression in the superior surface of the skull, as did the midbrain (Butler 1994). Hence, the thalamus was probably originally concerned predominately with visual stimuli and may have directed photopic information to both the brainstem and forebrain. In fact, the ancestral thalamus developed (via the epithalamus), a third photo-sensitive "eye" i.e. the pituitary/pineal eye. The pituitary/pineal eye first made its appearance about 400 million years ago with the evolution of the lamprey. Many ancient vertebrates possessed a parietal (third) eye, including creatures ancestral to modern reptiles, amphibians and fish (Colbert, 1980; Jarvik, 1980; Jerison, 1973; Romer, 1970).
Among more advanced vertebrates, the third eye has completely disapeared though the pineal gland has been retained. Nevertheless, the thalamus has remained visually responsive and through the geniculate nucleus, continues to receive, process, and transfer visual information received from the retinas as well as from the visual midbrain (Butler 1994; Casagrande & Joseph, 1978, 1980; Ebbesson, et al. 1972). Thus, although the human thalamus has lost its third eye, it continues to receive direct retinal input which is transmitted, via the optic radiations, to the occipital and inferior temporal and superior parietal lobes.
As noted, the hypothalamus, upon receiving pheromonal input via the vomeronasal organ became increasingly concerned with sexual and reproductive activities. However, this structure also began receiving increased visual input which was directed to the suprachiasmatic nucleus (SCN). The SCN not only become adapted to the daily cyclic rhythm associated with day and night, but acquired the capacity to secrete hormones and exert other influences on the brain in accordance with these daily rhythms. For example, the SCN appears to be the "master clock" for the generation of circadian rhythms; rhythms which have a period length of 24 hours (Aronson et al. 1993; Morin 1994).
However, if the SCN, for whatever reasons, fails to receive sufficient light, these circadian rhythms and associated hormonal secretions may become abnormal. As night is associated with reduced activity and sleep, under conditions of insufficient light and thus SCN abnormalities, patients may become lethargic and suffer from reduced energy and motivation; that is, they become depressed.
For example, the hypothalamic-pituitary axis secretes melatonin in phase with the circadian rhythm. Phase-delayed rhythms in plasma melatonin secretion have also been observed in many patients with this light sensitive form of depressed (see Wirz-Justice et al. 1993, for review). However, with light therapy, not only is the depression relieved but the melatonin secretions return to normal. This is significant for melatonin is derived from tryptophan via serotonin and low serotonin levels have been directly linked to depression (e.g. Van Pragg 1982). Moreover, the hypothalamus (and the midbrain) may act to regulate serotonin release (Chaouloff 1993), which in turn may explain why serotonin levels rhythmically fluctuate (e.g. such as during the sleep cycle), or become abnormal when denied sufficient light; i.e. the production of serotonin by the raphe nucleus (in the pons) is abnormally effected.
On the other hand, there is also some suggestion that abnormal temperature perception, or aging within the SCN may be responsible for the genesis of depressive in these cases. For example, age related changes in the SCN have been noted to adversely effect circadian rhythm generation as well as metabolic and peptide activity (Aronson et al. 1993). In consequence, rest vs active cycles also become abnormal, with reductions in arousal and activity; i.e. the patient becomes depressed.
By 360 million years ago a variety of five-toed amphibians, some up to 15 feet long were swarming over the planet. To accommodate the increased need for land-based motor control, further alterations occurred within the brainstem, cerebellum, thalamus, and striatal forebrain which expanded increasingly worked in tandem so as to initiate and coordinate species specific behavior patterns. In additon, the midbrain auditory and visual colliculi evolved feature detecting cells that could recognize specific prey by sight or sound. The midbrain also evolved the ability to visually mediate prey catching behaviors through specific motor programs and movements (Donkelaar, 1990). Hence, for a brief time amphibians "ruled" the world as they were more social, and more intelligent than those who had come before them.
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By 350 million to 300 million years B.P., the first reptiles appeared. Unlike their amphibious cousins, the reptiles were better engineered for living on dry land. For example, in addition to their scaly water proofed skins, they developed hip and shoulder girdles which improved their speed of movement and maneuverability. They also evolved a brain equipped with a well defined corpus and limbic striatum, and an expanded limbic system, whereas the hypothalamus was forced to develop new methods of thermoregulation in order to accomodate to life on dry land including additional nuclei that would prove the hormonal support for a "new" way of giving birth. In contrast to amphibians who must return to the water to breed and produce young, the reptiles could breed and lay amniote/cleidoic (shell covered) eggs on land from which emerged miniature adults.
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With the evolution of reptiles the lower brainstem also underwent additional differentiation and elaboration and unlike all previous creatures, reptiles began demonstrating mammal-like sleep periods (Ulinski, 1990). However, there is no evidence that reptiles experience "slow wave" or dream sleep. Living on land also necessitated additional evolutionary developments within the brainstem reticular formation, which began to resemble that of mammals (Newman & Cruce, 1982). Coupled with the ability to perceive sound, the extension and evolution of the reticular formation also contributed to evolution of the inferior auditory colliculus. With the evolution of these new midbrain capacities, amphibians and reptiles also gained the capacity to become aroused by and to oriented toward specific sounds.
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Moreover, with the progressive evolution of amphibians and then reptiles, the vestibular nucleus, inferior colliculi, medial geniculate thalamus, amygdala, and striatum also expanded and evolved the capacity not only to perceive sounds but to trigger orienting and alarm reactions in response to transient auditory stimuli -characteristics these nuclei retain even in modern primates (Edeline & Weinberger, 1991; Hitchock & Davis, 1991; Hocherhman & Yirmiya, 1990). Moreover, as the amygdala and striatum expanded the ability to perceive and display complex social emotional states also evolved.
THE REPTILIAN LIMBIC FOREBRAIN
With the evolution of reptiles, much of the amygdala had been completely displaced and was now ventrally located, whereas the hippocampus remained medially-dorsally situated (Gloor, 1997; Stephan & Andy, 1977; Ulinski, 1990). The striatum, however, remained as initially situated but in expanding became the ventral (limbic) and dorsal (corpus) striatum.
Specifically, it appears (as based on comparative neuronatomy) that the ventral aspect of the amygdala-striatum began to separate forming a distinct amygdala segment which remained ventrally located, and which extended along the ventricular floor, merging with the preoptic area as is the case in anurans (tailless amphibians). In mammals and humans, this ventral amygdala segment has twisted and rotated and has been pushed anteriorally, becoming the medial amygdala. Yet another amygdala segment initially remained somewhat dorsally situated (though still connected with the medial amygdala), becoming over the course of evolution (and as it rotated, shifted position and was pushed ventrally and anteriorally) the lateral amygdala.
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As the amygdala became reorganized to process secondary olfactory input including pheromonal chemical messengers transmitted by the vomeronasal organ (e.g., Bakker et al., 1996; Dudley et al., 1992), the main olfactory system also increased in size and increased its projections to the amygdala, and the hippocampus and hypothalamus (Stephan & Andy, 1977). Hence, all three limbic structures were directly influenced by olfactory/pheromonal cues, the hypothalamus responding emotionally, sexually, or with hunger, and the hippocampus comparing this data to previous impressions and related visual input, and then storing this information in memory.
As the hippocampus was also receiving visual input, it began to expand, becoming increasingly allocortical, forming (along with the amygdala) the piriform lobe. Moreover, the hippocampus began to give rise to mesocortical tissue, and what would eventually become the entorhinal cortex which covers portions of the hippocampus like a shroud and relays information to it and from it. Through the interactions of the entorhinal cortex and hippocampus, and in response to visual and olfactory input, the hippocampus gained the ability to integrate, learn and remember these attributes including their location in visual-olfactory space. The hippocampus became increasingly able to employ olfactory and visual cues in order to form a visual-olfactory map of the environment.
The amygdala also began integrating and storing these cues in memory. Moreover, it was able to act on these signals through connections still maintained with the striatum. Hence, just as the vomeronasal organ and olfactory system are involved in mediating the classic four "fs" feeding, fighting, fleeing, and sexual activity, as well as promoting social behavior; i.e. aggregating (Halpern, 1987) the amygdala became similarly organized and also became increasingly involved in regulating reproductive activities and in controlling the affective aspects of motor behavior via the striatum (MacLean, 1990).
THE EVOLUTION OF THE CIRCUITRY OF THE OLFACTORY LIMBIC SYSTEM
The vomeronasal organ projects to the hypothalamus as well as the amygdala The hypothalamus, therefore, also became increasingly responsive to pheromonal cues, especially in regard to sex, aggression, and feeding behaviors. In consequence, the connections between the hypothalamus and amygdala were also increased so that they could engage in coordinated action.
Likewise, since the visually responsive hippocampus/entorhinal cortex also received olfactory input, the connections between the amygdala and hippocampus were significantly expanded, and the hippocampus and hypothalamus also strengthened interconnections, thus forming the initial core of the limbic system which relied on the striatum and brainstem to act on its olfactory-triggered desires, urges and needs.
Now bound together in a common olfactory-limbic purpose, these structures could act in a coordinated fashion. The amygdala, upon detecting an emotionally significant stimulus, could act on the hippocampus, and together they could learn or generate appropriate memories. Both structures could also act on the hypothalamus so as to promote the generation of core emotional reactions including the secretion of necessary hormones and peptides. These structures could also act on the striatum so that appropriate behaviors related to feeding, fighting, fleeing, of sexual activity could take place.
The amygdala and hippocampus in particular, were also able to create an olfactory map of external reality and could not relate this to internal reality thus creating a separate internal and external reality, which in turn gave rise to personal reality, and an individual identity that was separate from the world and other creatures. Indeed, through olfactory cues, scent marking, an animal is able to advertise not only its personal, individual identity and status, but its personal possessions, such as its territory or sex partner.
Initially, the amygdala was joined to the striatum creating a single allocortical structure. However, as it was pushed apart, the medial amygdala remained closely associated with the striatum but was also receiving significant olfactory and pheromonal input. Consistent with its origins, the medial nuclei responds to olfactory input, but also analyzes auditory and visual and tactile stimuli transmitted to it from the brainstem and thalamus. If the stimulus is determined to be emotionally or motivationally significant, the medial amygdala, including that of cartilaginous fish, is able to trigger complex affective-motor movements, such as fleeing, fighting, feeding, or sexual behavior, and this is accomplished via the striatum and through joint projections to the brainstem.
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However, not only the amygdala, but the striatum split into separate structures, including the dorsally located caudate and putamen, and the ventrally situated limbic striatum. The dorsal striatum, however, ceased to receive olfactory input, whereas the ventral (limbic) striatum continued to. The limbic striatum, therefore, remained concerned with analyzing olfactory-related stimuli, as well as retaining this information, thus becoming a memory as well as a motor center that could act at the behest of amygdaloid influences. In contrast, the corpus striatum became increasingly concerned with affective-motor behaviors, including postural and behavioral displays associated with feeding, fighting, and sexual courtship. This was accomplished through major motor pathways, the "extra-pyramidal" system, which projected directly to the brainstem. Indeed, the striatum is the main motor output center of the forebrain (Donkelaar, 1990).
Thus the amygdala, through the striatum and via the dopamine neurotransmitter system, could now influence the more "hard wired" brainstem, so that the creatures emotional state could be expressed in a manner that was much more flexible and less reflexive. Thus in response to amygdala activation, the striatum could be stimulated in order to produce complex emotional displays, including those requiring rapid gross motor reponses, such as fleeing and fighting, via the brainstem (cf Heimer & Alheid, 1991; Mogenson & Yang, 1991).
The Amygdala, Striatum and Affective Motor Behavior
With the evolution of reptiles, a greater degree of complexity begans to typify male vs female sexual behavior and social-emotional behavior. Hence, the lateral (cortical) amygdala (which is concerned with complex sexual and social-emotional functions) began to evolve (Neary, 1990). Like the much more ancient central medial (and extended) amygdala, the lateral amygdala maintains rich interconnections with the hypothalamus and the preoptic area -nuclei concerned with sexual activities and male vs female sex specific behavior (see chapter 13).
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For example, with the evolution of reptiles, courtship displays became exceedingly complex and ritualized, with the male initially aggressively challenging the female (MacLean, 1990). He will signal her by swishing his tail rapidly back and forth and will aggressively nudge her along her side, even biting her neck if she attempts to run away--neck biting actually being a common courtship display even employed by sharks. Females of some lizard species also perform enticement displays. They will invite courtship by engaging in a form of flirting that entails inclining, arching, or nodding her head nodding, and as is more common among mammals and birds, she may then run away in order to entice the male to pursue. Moreover, once he catches her she may offer token or aggressive resistance--a form of foreplay which is also common among mammals including the human female (Ford and Beach, 1951).
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However, in order to display sex specific and other complex social affective behaviors, including those involved in the competition for and solicitation of mates, not only the amygdala and hypothalamus, but the limbic and dorsal striatum evolved accordingly. As noted, the striatum acts as the behest of the amygdala and produces complex social-affective motor behaviors including those involved in signaling dominance, aggression, fear and submission.
Lizard body language includes: 1) challange or territorial displays, 2) submissive and appeasement displays, 3) courtship displays, and 4) "signature" displays which often involve unique modifications that signify a degree of individuality (Maclean, 1990). By contrast, challenge, territorial, submissive, appeasement, and courtship display are highly ritualized and invariably involve head movements. For example, lizards will nod their heads as a form of greeting. However, if a lizard is confronted by an intruder into his territory he will respond with a challenge display. Stereotypically, he will begin doing pushup with his front legs, and may bob his head up to 12 times while simultaneously expanding his throat. If the intruder does not depart, the lizard will run towards him and turn sideways as he approaches. If the intruder still does not depart, the lizard may then lash him with his tail, or will engagin in pushing and shoving. If the intruder still does not depart, they may circle and may clamp their jaws on the others neck of tail, sometimes biting off the tail in the process. The challenge display will cease only when one of the combatants gives an appeasement display which consists of head bowing or by lying low on its tummy--behaviors which stereotypically displayed by many species of mammal. And as is common among non-human and human mammals (Ford & Beach, 1951), if this combat sequence is observed by a female, she may then attach herself to the victor.
The significance and implications of these behaviors are easily identifiable due to the fact that they are produced by a limbic system and striatum which has been inherited by mammals including humans; which is why similar behaviors are also displayed by these species.
However, over the course of evolution the striatum also expanded, and ioncreasingly contributed neurons to the external cortical layers that were slowly enveloping the old brain. In consequence, those cortical areas dorsal and anterior to the striatum also became concerned with affective motor functioning; especially in that they were also in receipt of neurons and axons contributed by the amygdala (as well as the hippocampus and thalamus). Thus, a rudimentary affective-motor cortex began to evolve, a portion of which would become, with the evolution of repto-mamals the anterior cingulate gyrus (MacLean, 1990).
However, because of their extreme importance in affective motor and social-affective behavior, if the striatum or overlying motor (cingulate) cortex are injured, the ability to motorically display affective states or to act on limbic motivational impulses is significantly curtailed and may be abolished.
As noted, in reptiles, the striatum is implicated in affective-motor displays involving the head and extremities. In humans, damage involving the corpus (dorsal) striatum can cause the face to become frozen and emotionless and the legs and arms to become rigid and stiff; e.g. Parkinson's disease. With massive lesions the individual may become catatonic and cease to move (see chapter 16). Similarly, the destruction of the amphibia and reptilian forebrain/striatum will disrupt species specific, and stereotyped social-emotional motor acts, such as dominance displays, or even the desire to eat and they may become catatonic (MacLean, 1990).
With forebrain/striatal destruction, reptiles and amphibians will cease to display or respond to emotional or motivational stimuli, including the presence of food, but instead will simply sit (MacLean, 1990). However, due to the preservation of the brainstem and cerebellum, if an frog with striatal destruction is turned over it will right itself, or if thrown into the water it will swim until reaching a dry surface where it again will simply sit. Indeed, if unmolested it will sit forever in the same spot, failing to demonstrate any desire to explore, eat, or have sex, until finally dying and becoming mummified (MacLean, 1990). As noted, in some respects this is reminiscent of the catatonia and loss of will that occur with massive striatal lesions involving the medial frontal lobes (chapters 16, 19).
Hence, with the evolution of reptiles, and the fully differentiated reptilian striatum, these animals were able to display complex social-emotional signals through body language, including dominance, submission, threat, sexual availability, and so on (MacLean, 1990). Reptiles were therefore more social, intelligent, and physically superior as compared to amphibians and via their expanded limbic system and corpus striatum, could employ complex postures and body language to communicate with rivals and members of the opposite sex.
Hence, in summary, the great expansion of the brain was a direct consequence of the increased importance of the olfactory system, with the brain expanding to accommodate olfactory needs. Much of the forebrain, therefore, is a derivative of the olfactory system which in turn induced the differentiation and reorganization of the amygdala-striatum thus creating an amygdala and striatum and contributing to the evolution of the hippocampus (Gloor, 1997; Stephan, 1983).
It is noteworthy that the original unity of the amygdala-striatum and its eventual separation is also repeated over the course of embrylogical development--yet another of the almost innumerable examples of ontogeny replicating phylogeny. For example, around the sixth week of fetal development immature neuroblasts migrate in massive numbers from the ventricular lining, and congregate in the more caudal portion of the emerging forebrain, thus forming an arc shaped "striatal ridge" from which the primordial amygdala will emerge (Gilles et al., 1983; Humphrey, 1968). However, approximately one week after the formation of the amygdala, this primordial amygdala-striatum begins to differentiate and balloon outward to create the striatum. That is, both the striatum and amygdala are derived from the arc shaped "striatal ridge," the caudal portion giving rise to the primordial amgydala at about the 6th week of gestation, and the basal portion later giving rise to the primordial striatum which initially overlies and is contiguous with the amygdala (Gilles et al., 1983; Humphrey, 1968). Over the ensuing weeks, these structures are pushed further apart thus again, replicating phylogeny. Moreover, just as olfactory influences are important in the evolutionary differentation of these structures, so to are olfactory influences important in embyology and the formation and development of the forebrain (Joseph, 1998d).
It is also due to the olfactory origins which enabled the forebrain to develop memory and the ability to think before reacting. Hence, in contrast to the brainstem which is not only more "hard wired" but which responds reflexively to proximal stimuli, the forebrain became adapted for analyzing and responding to both proximal and distant stimuli, as conveyed via olfactory cues. These differential sensitivities provided the olfactory-limbic forebrain with an intellectual and nmemonic evolutionary advantage over the midbrain and brainstem in regard to the development of thinking, planning, and memory. That is, since olfactory stimuli tend to arise in the distant environment, this gives the organism more time to analyze these signals before responding. Hence, being the recepient of this distant information, the forebrain was given time to "think", whereas the brainstem in response to tactile, painful stimuli, had to react immediately and reflexively. Moreover, because the source of this chemical/pheromonal information might be far away and hidden, the forebrain had to retain this information in "memory" for long time periods, or for however long it took to approach or get away.
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In that the brainstem and the thalamus also relayed sensory data to the forebrain (Butler 1994; Donkelaar, 1990), the forebrain became increasingly specialized for interpreting and associating multiple sensory signals simultaneously, and was able to "think" about what actions to take, and/or store this information in memory so as to "think" about or act on it later. By contrast, the brainstem continued to reflexively act in a stereotyped and unthinking manner. As the hypothalamus is in part an outgrowth and intimately associated with the midbrain, although also part of the limbic system, this diencephalic structure also tends to react reflexively. However, as the hypothalamus is also intimately interconnected with the amygdala, and as these pathways became more robust, the amygdala in turn acquired the ability to influence and exert some degree of control over this more primitive emotional center. Initially, however, the hypothalamus appears to have been predominant, such that creatures such as sharks, although possessing a forebrain that could think, also largely react in a reflexive manner.
The Reptile to Repto-Mammal Neurological Transition
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Primordial reptiles split into three lineages, the anapsids which gave rise to modern turtles, synapsids which gave rise to reptomammals and then therapsids, and diapsids which gave rise to dinosaurs, and birds, and present day reptiles.
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With the evolution of reptiles, pallial neurons migrated to the dorsal portion of the striatal hemisphere to form the first true albeit simple three layered cortex. However, the ventral pallium remained similar to that of amphibians. Yet other pallial neurons, those medially located, instead began to proliferate and to form large masses of gray matter that began to bulge into the lateral ventricle, thus forming the dorsal ventricular ridge. The dorsal ventricular ridge is homoplastic with the mammalian striatum.
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In birds, reptiles, and saurosids, the dorsal ventricular ridge gave rise to the neostriatum and hyperstriatum, and thus a pattern of cerebral organization quite different from mammals (Ariens Kappers et al., 1936; Parent & Olivier, 1970). That is, whereas the pallium of birds and reptiles developed inward (i.e. outside in) so as to form the dorsal ventricular ridge, the pallium of repto-mammals, therapsids, and mammals, expanded from inside out, to form allocortex, then mesocortex and then neocortex, with primitive and complex modern day mammals, e.g. marsupials, placentals, displaying all three cortical patterns; i.e. within the limbic system, cingulate gyrus, medial and uncal temporal lobe.
REPTO-MAMMALS AND THERAPSIDS
Reptiles evolved multi-regionally, a variety of species appearing on almost every continent. However, around 250 million years ago, and corresponding with major climatic changes, a more advanced species of reptile emerged, the repto-mammals (Brink, 1956; Broom, 1932, Crompton & Jenkins, 1973; Paul, 1988; Romer, 1966). Although more reptile than mammal, the repto-mammals represented a tremendous leap in intellectual and physical prowess. For example, the repto-mammalian brain now included an enlarged basal ganglia and corpus and limbic striatum, whereas the new three layered cortical area devoted to affective motor functioning, added a new layer to become a rudimentary anterior cingulate gyrus (Joseph, 1993; Maclean, 1990). Coupled with the development of a mammal-like striatum, the emergence of the anterior cingulate provided these creatures with the capacity to engage in complex social-emotional behaviors, to vocalize a variety of social-emotional affective states, and to display prolonged maternal care (Joseph, 1993; MacLean, 1990).
The emergence of these creatures represented a giant leap in physio-technological and neurological capability. They dwarfed all previous creatures in complexity, intelligence and physical prowess for important physical alterations occurred not just in their brains but in their body structure, stance, gait, and limb development (Colbert, 1980; Jarvik, 1980; Jerison, 1973; Romer, 1970). For example, the legs were now located beneath rather than alongside the body which enabled them to run long distances without compressing the chest and lung which allowed them to simultaneously breath while chasing prey. Reptiles must stop in order to breath since their legs, situated alongside their body and chest cavity, constrict the expansion of the lungs as they run.
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The repto-mammals also developed a secondary bony palate which enabled them to chew food and to simultaneously breathe without danger of choking to death. Reptiles must cease to breathe in order to swallow large chunks of their food.
Another advantage occurred in regard to thermoregulation. Repto-mammals became warm blooded and the hypothalamus and limbic system evolved a means of regulating body temperature internally. Moreover, whereas lizards, frogs, fish, etc., have only scales, the therapsids evolved a coat of fur, as well as sweat glands that released excessive internal heat. By contrast reptiles must sun themselves to gain heat, or sit in the shade to cool off, and are thus forced to rely on behavioral thermoregulation. For example, if a reptile fails to move from a cold to a warm location (or vice versa) their body temperature soon approaches that of the external environment.
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In addition, therapsids appear to have evolved a "double pump" heart and the formation of a interventricular septum which induces a total separation of deoxygenated and oxygenated blood.energy. The acquisition of these metabolic capabilities, also increased aerobic metabolic power which led to the development of endothermy. Endothermy is the capacity to increase the production of endogenous metabolic. Hence, whereas reptiles and amphibians are extotherms, therapsids, and presumably repto-mammals became endotherms.
Thus therapsids and eventually mammals, gained the capacity to sustain physical activity at high levels as they now had increased tenfold their ability to engage in aerobic oxidative metabolism. Indeed, metabolic rates are up to 10 times higher in endotherms vs ectotherms, which enables endotherms to engage in prolonged energy consuming activities, and when necessary, can still increase yet further their activities such as speed of running, anaerobically and aerobically. Reptiles are capable of engaging in only short bursts of activity. However, they must quickly slow and stop, and due to the buildup of lactic acid and the loss of high energy phosphate, recovery can take hours such that they slow and then become motionless.
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Thus the initial evolution of the repto-mammals coincided with and resulted in major biological alterations involving cranial and post-cranial skeletal structure, mammillary development, thermo-regulation, sexual reproduction, and hypothalamic function and structure (Bakker, 1971; Brink, 1956; Broom, 1932, Crompton & Jenkins, 1973; Duvall, 1986; Joseph, 1993; Maclean, 1990; Paul, 1988; Quiroga, 1980; Romer, 1966). Hence, the Repto-mammals were now able to roam and explore vast new territories, and in so doing they proliferated and a tremendous diversity of forms were unleashed upon the planet (Bakke, 1971; Brink, 1956; Crompton & Jenkins, 1973; Crompton, et al. 1979; Duvall, 1990; Maglio, 1978; Romer, 1966; Quiroga, 1979). Indeed, the remains of repto-mammals have been found on every continent including Antarctica. They not only assumed dominion over the Earth, but ruled over even the first tiny dinosaurs (the theocondants), who appeared around 225 million years ago.
However, the Earth was apparently struck by two giant meteors around 250 million and 225 million years B.P., an event which ended the dominion of the repto-mammals and which resulted in a mass extinction of life on land and in the sea (Raup, 1991; Stanley & Yang 1994). Since larger creatures (i.e. the repto-mammals) were more severely effected, this event led to the ascendance of the (initially very small) dinosaurs who soon grew to huge sizes.
This forced the remaining and now much smaller species of repto-mammals to adapt to a whole new way of living, including nighttime foraging. This new lifestyle, however, resulted in improved auditory, and olfactory-pheromonal functional capacities but diminished the importance of vision.
Over the next 100 million years due to their new lifestyle and the competitive pressure and presence of the dinosaurs, the repto-mammals became smarter, and their brains became larger and more complex, such that they became increasingly mammalian. Repto-mammals thus became therapsids.
There were two main suborders of therapsids, the Theriodontia (who were carnivores) and the Anomodontia (which were herbivores). Some scientists believe that true mammals descended from Theriodontias, whereas others suggest that carnivores gave rise to carnivores and herbivores to herbivores including modern day monotremes.
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The lines leading from repto-mammals and therapsids to monotremes and marsupials mammals, must have split off well over 150 million years ago, giving rise to distinct marsupials and monotremes by around 100 million years ago, and from separate branches, to plancentals. Placentals included the first insectivores, as well as credonta, carnvoria, and the first primitive primates (Novacek, 1992).
Like reptiles, monotremes (duck-billed platypus and spiny enchidnas) lay eggs, and like birds they have evolved horny toothless beaks. Unlike modern mammals such as carnivors and primates, the monotreme brain consists of only 3 or 4 visual areas, compared with over 20 for carnivores and primates.
However, within that branch or intermediate mammals referred to as marsupials, there are numerous intermediate mammalian representatives, that markedly resemble their more advanced plancental cousins; e.g. gliders which resemble flying squirrels.
Placentals are distinguished by have a placenta which enables a mother and her fetus to exchange gasses and nutrients. Placental mammals are obviously more advanced as is also indicated by the fact that they are the dominant mammalian life form, comprising over 20 orders.
In any case, the therapsids became increasingly mammal like in regard to their skull, teeth, the formation of a middle ear, and in regard to their locomotor skeleton. For example, in contrast to reptiles and amphibians, the elbows were now directed backward and the knees forward which greatly improved their ability to run and manipulate their limbs.
However, whereas the Theriodontias were likely giving live birth to infants that required prolonged maternal care, the hervivorous therapsids appear to have been egg layers. For example, monotremes appear to be the direct descendants of the Theriodontias and they too are egg layers. These primitive modern mammals include the anteaters and the duck billed platypus. Moreover, like therapsids, they suckle their young via modified sweat glands which secrete milk and which correspond to the mammarly glands of of other mammals. The monotremes, in fact, appear in the fossil record as far back as the earliest periods of the Pleistocene.
Like modern day mammals, including monotremes, therapsids engaged in prolonged maternal care, and the young lived with their mother until they became juveniles. These adaptions in turn appear to have been made possible via major alterations in the brain, as well as the middle ear, which, in repto-mammals was still part of the jaw. Therapsids evolved the malleus and incus which, coupled with other changes, enabled them to perceive a variety of frequencies. Moreover, the five layered anterior cingulate appears to have fully emerged, which, when coupled with advances in the striatum, enabled these creatures to employ gestures and posturing as well as produce a variety of complex emotional sounds in order to communicate. Indeed, it was likely the evolution of the anterior cingulate, coupled with the ability to produce complex sounds (such as the infant's separation cry) promoted prolonged child care as well as the development of language and the family (Joseph, 1993; MacLean, 1990). [-INSERT FIGURES 51 & 52 ABOUT HERE-]
THE EVOLUTION OF THE SEPTAL NUCLEI AND CINGULATE
With the evolution of repto-mammals, over 250 million years ago, and then therapsids 200 to 150 million years ago (e.g. Probainognathus from the triassic followed by Periptychus from the Paleocene), the olfactory bulb greatly expanded as did the amygdala-hippocampus-containing piriform lobe (Quiroga, 1980; Ulinksi, 1990) which came to dominate and form the largest structure (or lobe) of the forebrain. Even in primitive mammals, the piriform lobe and the other primary olfactory structures, forms the largest portion of the hemisphere including much of the lateral surface.
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With the evolution of repto-mammals the medial portions of the brain still contained the dorsal medial hippocampus which in turn became slowly transformed so as to analyze and process the increased level of sensory input being received. Like the amygdala the hippocampus was also being pushed and stretched in different directions, the medial portions (through which interconnections with the hypothalamus were maintained) becoming tissue thin, and the ventral aspects becoming enlongated. However, in this regard, the hippocampus had already begun to contribute to the evolution not only of the medial walls of the hemisphere, but to the emergence of the septum pelucidum and thus the septal nuclei which was simultaneously emerging and being yanked out of the hypothalamus by the departing hippocampus.
Over the ensuing 100 million years, and with the evolution of the therapsids, the dorsal-medial three layered allocortex was becoming four then five layered mesocortex, thus forming what would become the cingulate gyrus (MacLean, 1990). The cingulate gyrus not only crowned the forebrain, but was a crowning achievement in the development of complex social emotional relationships, including long-term maternal behavior, and what would eventually become the "family" and modern human speech.
THE ANTERIOR CINGULATE, MATERNAL BEHAVIOR AND EMOTIONAL SPEECH
The most prominent nuclei of the midbrain include the superior (visual) and inferior (auditory) colliculi. These structures are concerned with analyzing visual and auditory signals, such as sudden movements or transient sounds, and can orient the head and body toward the source of stimulation (via it's extensive interconnections with the brainstem reticular formation and motor nuclei). Via interconnections with the amygdala and striatum, these auditory and visual signals could also be analyzed in regard to emotional significance and appropriate action could then be initiated.
As noted, it is the striatum which guides and controls affective-motor behaviors (e.g. kicking, flailing, biting, running), in response to amygdaloid input. However, the amygdala not only perceives emotional stimuli and stimulates appropriate affective-motor behaviors, but it can also produce complex social-emotional vocalizations via connections with the striatum as well as the midbrain periaqueductal gray.
When repto-mammals evolved, the amygdala, striatum, as well as the hippocampus contributed to the evolution of the affective-motor cortical area that was to become the five layered mesocortical, anterior cingulate. Over the course of evolution, the anterior cingulate expanded and developed five layers, three of which were sandwiched between layers I and V which had been originally contributed by the midbrain. As the anterior cingulate evolved, it thus became increasingly concerned with affective motor behavior, including the production of emotional vocalizations which were emitted in concert with the amygdala and via interconnections with the midbrain periaqueductal gray.
The evolution of the cingulate gyrus coincided with the emergence of the therapsids and thus ushered in a stage in evolution where sound came to serve as a means of purposeful and complex communication, such as occurs not only between potential mates, sexual competitors, or predator and prey, but between mother and infant (Joseph, 1993, 1999b; Maclean, 1990). In fact, the most recently evolved five layered transitional limbic cortex, the (anterior) cingulate gyrus, is exceedingly vocal, and can produce sounds that do not correlate with mood, indicating considerable flexibility and plasticity within this structure (Jurgens & Muller-Preuss, 1977). The cingulate is not only capable of producing a complex medley of emotional sounds, but the separation cry, which is similar if not identical to that produced by an infant (MacLean, 1990; Robinson, 1967). It is these particular sounds which promote intimate maternal behavior and which promote the establishment of emotional attachments (Joseph, 1999b).
In fact, it is with the evolution of the repto-mammals and therapsids that prolonged maternal care became the norm. For example, the scent glands became mammilary glands; i.e. the maternal nipple, such that the capacity to nurse came into being (Duvall, 1986) whereas the young would live with their mothers until they reached the juvenile stage. As these events corresponded to the evolution of the anterior cingulate, and as this structure promotes maternal behavior and attachment, it thus appears that evolution of the cingulate promoted the development of the family.
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By contrast, as has been repeatedly demonstrated in humans and lower mammals, anterior cingulate destruction can result in a loss of maternal responsiveness and can significantly impair if not abolish the production emotional-prosodic vocalizations thus resulting in mutism (Barris & Schuman, 1953; Kennard, 1955; Laplane et al. 1981; Smith, 1944; Tow & Whitty, 1953). In primates maternal behavior is also abolished and the majority of infants whose mothers have suffered anterior cingulate destruction, soon die from lack of care. In fact, mother may walk upon their infants as if they were inanimate objects; that is, behavior becomes reptilian.
The Limbic System and the Evolution of Emotional Attachment
Sharks, teleosts, amphibians, and reptiles (although lacking a cingulate gyrus) possess a limbic system, consisting of an amygdala, hippocampus, hypothalamus, and septal nuclei. It is these limbic nuclei which enable a group of fish to congregate and "school", and which makes it possible for reptiles to form territories which include an alpha female, several sub-females, and a few juveniles (Joseph, 1993; Maclean, 1990). It is also these structures which enable some of these creatures to produce an exceedingly limited repertoire emotional sounds, such as those indicating pleasure or distress, including shrieks and cries of alarm.
It is noteworthy, however, that vocalizations triggered by excitation of the amygdala, hypothalamus, or septal nuclei are usually accompanied by appropriate, and mood congruent behaviors (Gloor, 1960; Jurgens, 1990; Robinson, 1967; Ursin & Kaada, 1960). In contrast, the cingulate gyrus is capable of considerable emotional flexibility and can trigger a variety of vocalizations that do not correspond to mood, including, for example, the production of sounds or behaviors that may fool a predator into thinking a potential prey is injured, when in fact it is a mother pretending to be disabled so as to distract a predator from her young. Again, the anterior cingulate is directly implicated in the generation of long term emotional attachments, in particular those between a mother and her young.
By contrast, sharks, bony fish, amphibians and most but not all reptiles show little or no maternal care and will greedily cannibalize their infants who in turn must hide from their parents, in order to avoid being eaten (MacLean, 1990). And yet, although lacking a cingulate gyrus, fish will school, and reptiles may form territories that include an alpha male, a female, and several juveniles. These behaviors, however, are a function of the amygdala which promotes group but not individual attachments (chapters 13,15,28).
Hence, in contrast to reptiles and amphibians, the repto-mammals and therapsids were equipped with recently evolved cingulate cortex, and not only lived in packs and social groups, but formed long term individual attachments between a mother and her young (Bakker, 1971; Brink, 1956; Crompton & Jenkins, 1973; Duvall, 1986; Paul, 1988; Romer, 1966). Being equipped with an amygdala, septal nucleus, as well as a cingulate gyrus, social and emotional relationships therefore became long term.
It is these same limbic nuclei which enable human infants to initially indiscriminately seek social and physical contact, and to then increasing display fear of strangers and to form specific attachments -events which correspond with the maturation of the amygdala followed by the septal nuclei and the cingulate gyrus (see chapters 15, 28). It is also the interaction and maturation of these limbic system structures which provide the neurological foundations not only for affective speech, but those neocortical substrates which would eventually give rise to modern human language.
The Piriform & Entorhinal Cortex
With the evolution and growth of cingulate cortex, the hippocampus was further dislodged and became elongated and stretched arc-wise, thereby forming dorsal-medial and ventral components. Pushing and dragging the emerging entorhinal cortex before and after it, the ventral most aspect of the hippocampus also carried with it the posterior portion of the piriform lobe which began to collide with the amygdala and the anterior portion of the piriform lobe; the collision taking place at the junction of the uncus.
As based on endocasts and comparisons to modern "living fossils" it appears that in response to increased olfactory, visual, and auditory input (around 150 million years ago) that the hippocampal half of the piriform lobe continued to sprout four to five layered mesocortex giving rise to the posterior cingulate, as well as what would become the six to seven layered entorhinal cortex--the "gateway to the hippocampus." The entorhinal cortex (a major memory and memory relay center) was carried with the hippocampus as it was pushed anterior-ventrally along with the amygdala (that is, due to continued expansion of the brain).
Likewise, it appears that the amygdala began to litterally spin out mesocortex which began to overlay portions of the allocortex. In consequence, over the ensuing 50 million years, that is by 100,000 B.P., the brain consisted not only of allocortex and mesocortex, but a combination of the two, thereby creating the piriform lobe and the six to seven layered entorhinal cortex and the beginning of a neocortical shroud that would become the temporal and orbital frontal lobes.
THE EVOLUTION OF MAMMALIAN NEOCORTEX: THE TEMPORAL LOBE
For much of neurological evolution, the olfactory-amygdala- hippocampus dominated forebrain functioning--as is evident from the size of the piriform lobe. Moreover, for much of early mammalian evolution, the olfactory-forebrain continued to dominate cerebral and cognitive functioning (Gloor, 1997; Haberly 1990). According to Gloor (1997, p. 54), "the earliest development in mammalian brain evolution seems to have been a growth spurt of olfactory telencephalon. The isocortex in these forms sat like a small cap on top of a very large olfactory telencephalon."
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Hence, by 100,000 years ago, the piriform lobe and cingulate gyrus appear to have been capped by a small nub of neocortex (Quiroga, 1980). Over the next fifty million years this neocortical cap soon became a shroud and enveloped the hemispheres of the telencephalon and the right and left piriform lobe, thus forming a very rudimentary temporal lobe--a structure which consists of allocortex, mesocortex, entorhinal cortex, and neocortex and which contains the amygdala and hippocampus, the core components of the limbic system.
Over the course of later mammalian evolution and as these creatures gained complete dominion over much of the planet, the neocortex began to expand at a rapid rate (Stephan & Andy, 1977). In fact, when comparing the brains of "living fossils" such as insectivores with that of humans, it appears that the neocortex expanded by a factor of 156 (even when taking into account differences in body size), whereas allocortex and mesocortex and all associated olfactory-limbic structures developed at a much reduced rate such that the hippocampus and septum are only 4 times larger and the amygdala is 6 times larger when comparing humans to insectivores, whereas the olfactory bulb is 40 times smaller (Stephan & Andy, 1969; Stephan, 1983). Indeed, not only does the olfactory bulb shrink with the evolution of humans, but the vomeronasal system has become vestigial.
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Specifically, during the end of the therapsid rein, some 150-100 million years ago, and during the therapsid mammalian transition, the brain begins to resemble that of a opossum or hedghog-- as is evident based on endoasts of later appearing therapsids, e.g. Phenocodus. Thus the lissencephalic surface area of the brain consisted of allocortex, mesocortex, entorhinal cortex, and neocortex. However, in the opossum, the piriform lobe continues to make up almost two thirds of the hemisphere, and in insectivores, half of the hemisphere consists of olfactory structures (Herrick, 1925; Quiroga, 1980; Stephan & Andy, 1977;). Hence, with the emergence of mammals, the cerebrum was still dominated by the olfactory system and the three and five layered allocortex and mesocortex, coupled with an expanding entorhinal cortex and a small nubin of neocortex.
As noted, the hippocampus was initially dominated by visual input, which later became supplanted by olfactory input. Nevertheless, this structure remained visually responsive and continued to perform visual-related functions which were superimposed with that of the olfactory system. That is, the hippocampus created visual place maps which became visual-olfactory maps that enabled animals to navigate through their environment as well as remember why they were moving about in the first place. However, with the reduction in the importance of olfactory input and the ascendance of visual sensation, the hippocampus and its overlying shroud of entorhinal cortex became dominated by the visual modality (Gloor, 1997). In fact, with the evolution of mammals, the entorhinal cortex formed the visually responsive "occipital" pole of the hemisphere.
As the brain began to rapidly expand, the hippocampus also began to expand caudally, medially, and laterally, thus becoming a dorsal and ventral hippocampus (bordered caudally by the evolving entorhinal cortex) thus forming the caudal portion of the piriform lobe. As it and the entorhinal cortex were pushed anterior-ventrally, they not only contributed to the evolution of the posterior cingulate, septal nucleus, and medial walls of the hemisphere, but to the evolution of the visually responsive occipital neocortex as well as the temporal lobe (Herrick, 1925; Nieuwenhuys & Meek, 1990ab; Quiroga, 1980; Stephan & Andy, 1977). Likewise, the amygdala, as it expanded and separated from the striatum, began to form the anterior portion of the piriform lobe, and the anterior cingulate (via the amygdala-striatum) as well as the temporal lobe.
Specifically, with the evolution of mammals and then primates, and due to the posterior-caudal trajectory of growth of the hippocampus and amygdala, including the piriform lobe and entorhinal cortex, these structures gave rise to and become enmeshed within the temporal lobe (Herrick, 1925; Nieuwenhuys & Meek, 1990ab; Quiroga, 1980; Stephan & Andy, 1977; Ulinksi, 1990). In addition, the entorhinal "occipital" lobe was pushed ventrally and forward, such that the occipital lobe came to be completely occupied by neocortex--six to seven layered neocortex which appears to have been "secreted" by the departing seven to eight layered entorhinal cortex. Moreover, neocortex followed the entorhinal cortex as it was pushed anteriorally ventrally thus forming the neocortical surface of the temporal lobe.
Likewise, the amygdala also contributes to the evolution of neocortex, such that anterior folds of neocortex coalesces with the posterior folds, and in the process creates distinct cytoarchitectural areas that are specialized to process different forms of information, i.e. auditory (amygala) vs visual (hippocampus). That is, the amygdala litterally began to rotate and spin over the course of evolution, giving rise to outflowing streams of increasingly cortical tissue--much like lava erupting from a volcano. Thus the amygdala gave rise to allocortex which formed part of the uncal foundation of the temporal lobe, over which flowed mesocortex, and then lastly neocortex, which then began to flow laterally, medially, and anteriorally, creating auditory cortex. The neocortex created by the amygdala was joined by those visually responsive neocortical streams flowing from the posterior portions of the brain, in the wake of the entorhinal cortex and the underlying hippocampus which also pushed the amygdala before them. In consequence, the "head" of the hippocampus also came to envelop part of the amygdala at the junction known as the uncus (Gloor, 1997).
The uncus (hook) is a structure almost unique to humans, and it is unique in that it is comprised of allocortex, mesocortex, entorhinal cortex, and includes portions of the amygdala and hippocampus. It is at the junction of the uncus where the amygdaloid gray and the entorhinal/hippocampus came to butt together. Hence, the periamygdaloid portion of the uncus represents the cortico-amygdala transition area which acts as a boundary against which abutts the entorhinal mesocortex.
Hence, whereas the evolution of the five layered mesocortical cingulate gyrus is one of the major distinguishing features of the evolution of the repto-mammalian brain, the creation of neocortex and in particular the temporal and occipital lobes, are the major distinguishing features heralding the transformation of therapsids into mammals and mammals into primates.
THE EVOLUTION OF MAMMALIAN NEOCORTEX
The demise of the dinosaurs, enabled mammals to gain dominion over the day as well as the night. And it was only during the ensuing evolution of primates, monkeys and apes in particular, that the olfactory dominance came to be challenged and reduced and supplanted by visual and auditory input which became dominant. Likewise, olfactory input into the hippocampus was almost completely eliminated, being directed instead to the entorhinal cortex. Hence, the hippocampus also became dominated by visual input (and less so auditory input).
Whereas olfaction was the driving force that transformed the reptilian brain into a repto-mammal and then a therapsid brain equipped with cerebral hemispheres (Herrick, 1925; Nieuwenhuys & Meek, 1990ab; Quiroga, 1980; Stephan & Andy, 1977; Ulinksi, 1990), it is with the emergence of auditory and visual functioning as the dominant sensory modalities, that provided the impetus for the great expansion and evolution of the temporal lobe. However, although temporal lobe structures are apparent in some mammals, such as dogs and wolves, only primates possess a true temporal lobe; a consequence of the expansion of the visual system and, to a lesser extent, an expansion of the auditory system.
Visual processing assumed increased importance only with the demise of the dinosaurs. Thus primates were able to emerge from the underbrush and the darkness of night, and by 55 million years ago, during the early Eocene, at least some orders of primates (e.g. Tetonius) had already evolved a large occipital, as well as an emerging temporal lobes (Radinksy, 1967, 1970)--brains which resemble those of modern day prosimians such as the Galago, as well as modern day carnivores such as wolves and dogs.
With the evolution and expansion of the temporal lobe and the auditory and visual areas, the hippocampus also expanded and acquired the capability of regulating cortical arousal and information processing--a capability which it then began to relinquish once the frontal lobe began to expand. That is, the expansion of the frontal lobe lagged behind that of the temporal lobe (see chapter 6).
As we ascend from "primitive" mammals (as represented by opossums, insectivores and hedgehogs) the poorly differentiated thalamus, and the diffusely (albeit crudly topographically) organized and overlapping primary sensory and motor areas, and the exceedingly small nub of association cortex (Diamond & Hall, 1969; Kaas et al., 1970; Ulinksi, 1990), expands and becomes increasingly differentiated, segregated and distinct, with numerous association areas sprouting throughout the neocortical surface of the hemispheres, and with distinct thalamic and neocortical areas becoming specialized to process different aspects of auditory, somesthetic, and visual information. Thus with mammals, the isocortex is dominated by detailed sensory maps of external reality, whereas in reptiles and amphibians, detail is provided only by the midbrain tectum.
In primitive mammals, piriform lobe (within which is partly contained the amygdala and hippocampus) and the other primary olfactory structures, form the largest portion of the hemisphere including much of the lateral surface. However, over the course of primate evolution, the expanding neocortex wraps itself around and also erupts from the piriform lobe which in turn becomes.
incorporated into the temporal lobe thereby forming the uncus (Herrick, 1925; Stephan & Andy, 1977). Morphologically, the mammalian including the human temporal lobe is the most heterogenous of all the lobes, particularly in that it contains a significant amount of allocortex (Vogt & Vogt, 1919); i.e. the 3 layered mesial and basal areas of the hemispheres which forms the hippocampal and piriform, periamygdaloid cortices.
Allocortex is thinner than neocortex and consists of 3 layers, and the large pyramidal cells of the second alocortex layer are more densely packed together as compared to any of the 6 to 7 neocortical layers. Whereas neocortical layers alternate between granular and pyramidal cells, allocortex is predominantly pyramidal cells.
Hence, within the temporal lobe, there is also a transition from allocortex to mesocortex, to isocortex (neocortex) with the medially located entorhinal cortex consisting of 7 to 8 layers. The medial mesocortex includes the entorhinal and posterior parahippocampal cortex (the parahippocampal gyrus) and extends from the anterior uncal regions in a belt-like fashion, extending through the dorsal surface of the temporal lobe, enters the insula, where it swings around and continues into the orbital frontal region.
THE EVOLUTION OF THE AUDITORY NEOCORTEX
Over the course of evolutionary metamorphosis, the olfactory forebrain, including the amygdala, septal nuclei, hippocampus, and striatum, became more complex and began developing additional layers of nerve cells which in turn contributed to the expansion of the forebrain/telencephalon. For example, as the medial amygdala expanded it became increasingly cortical thus forming the uncus of what would become the temporal lobe and then later contributed to the evolution of the auditory neocortex. Indeed, the amygdala receives auditory stimuli from the medial geniculate and the inferior colliculus and in lower mammals is exceedingly responsive to auditory input, whereas the human amygdala is responsive to complex auditory-affective stimuli including words and sentences (Halgren, 1992; Heit, Smith & Halgren, 1988). If electrically stimulated, patients report hearing voices which tend to be experienced as emotionally significant (Gloor, Olivier, & Quesney, 1981).
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Hence, over the course of evolution, the amygdala continued to expand, contributing pyramidal neurons which sandwiched themselves between what would later become layers I and VII of the neocortex, and in so doing also contributed to the evolution of the auditory neocortex with which it remains extensively interconnected via the inferior arcuate fasciculus. In fact, immediately beneath and buttressing the auditory neocortex is a thick band of amygdala-cortex, the claustrum. Over the course of evolution the claustrum apparently split off from the amygdala due to the expansion of the temporal lobe and the passage of additional axons coursing throughout the white matter (Gilles et al., 1983). Nevertheless, the claustrum maintains rich interconnections with the superior auditory cortex as well as the amygdala (Gilles et al., 1983). However, the amygdala is not only responsive to auditory input, but is one of the most vocally responsive structures of the brain (Jurgens, 1990, 1992; Robinson, 1967, 1972) as it is directly connected with the midbrain periaqueductal gray, and the anterior cingulate--a structure whose evolution was also promoted by the amygdala.
Hippocampal Contributions to the Neocortical Evolution
Over the course of vertebrate evolution and with the transition from amphibian to mammal, the medially situated septal nuclei and hippocampus contributed to the development of the cingulate gyrus, including the medial walls of the neocortex, with the hippocampus promoting the evolution of what would eventually become the posterior cingulate, and the medial parietal, occipital and temporal lobes (Herrick, 1925; Nieuwenhuys & Meek, 1990ab; Quiroga, 1980; Stephan & Andy, 1977).
Because the hippocampus was predominantly concerned with visual stimuli, the parietal, occipital, and temporal lobes became similarly organized. Moreover, because the hippocampus was also concerned with memory, the temporal lobe became similarly organized. And, as the hippocampus was also concerned with mapping the location of objects including one's body in visual space, the parietal lobe became similarly organized.
Cingulate Contributions to Neocortical Evolution
As per the evolution of the anterior cingulate, yet another contributor to its evolution was the striatum. In addition, both the cingulate and the striatum promoted the evolution of the frontal and parietal neocortex. For example, the anterior cingulate, being in part, motor cortex, appears to have given rise to the medial frontal motor areas (Sanides 1964), and that over the course of evolution, it continued to expand upward and then laterally thus forming the superior and the lateral frontal motor areas, including Broca's speech area in the left frontal lobe and the emotional melodic speech area in the right frontal lobe--both of which remain extensively interconnected with the anterior cingulate.
Midbrain Contributions to Neocortical Evolution
Yet other contributors to the evolution of the neocortex include the thalamus and the midibrain. For example, the thalamus is richly interconnected with and appears to have donated neurons to layer IV. However, it appears that the midbrain may well have provided much of the foundation for the neocortex by providing layers I and VII (also referred to as VIb). Indeed, layer I generally lacks neurons, and is phylogenetically old in structure and composition and has a similar organization among all vertebrates except fish (Marin-Padilla 1988a).
As noted, layers I and VII (VIb) appear to exert an attractive influence on migrating neurons during embryological development, which sandwich themselves between these layers thus forming layers II through VI. Hence, over the course evolution, as various forebrain structures expanded and/or became increasingly cortical, they too contributed neurons that sandwiched themselves between these layers--an evolutionary process which, being under genetic control, is now accomplished during embryological development.
For example, layer 1 appears to maintain an intimate relationship with the reticular activating system (Marin-Padilla 1988a), as well as the norepinephrine (NE) transmitter system, perhaps acting as their most distal component. NE, however, promotes neural plasticity and growth, whereas the reticular activity system is excitatory. In this regard, layer 1 may provide a low threshold background of excitation and growth promoting influence which acts to attract migrating neurons. Upon arriving, these neurons penetrate layer VII in order to reach layer I, with each successive wave forming successive layers II through VI, thereby creating a 7 layered neocortex.
THE EVOLUTION OF THE NEOCORTEX
Over the course of evolution, the transition form allocortex to neocortex is rather gradual--and this is also reflected in the modern temporal lobe which is belted by a dysgranular intermediate cortex, variably referred to as "transitional," "paralimbic cortex," "paleocortex" and "mesocortex." The cingulate, for example, consists of "mesocortex," whereas the entorhinal cortex is both allocortex (3 layers) and mesocortex (4 to 5 layers) and thus consists of 7 to 8 layers. The unique 7 to 8 layered organization of the entorhinal cortex probably reflects its exceptional status as an assimilation cortex that receives, integrates and relays information from the association areas to the hippocampus and back again (Gloor, 1997).
Hence, whereas the entorhinal cortex consists of 7 to 8 layers, the neocortex, consists of six to seven layers. The thickness of these layers, as well as the size of their neurons, and thus of the neocortex, also varies depending on brain region, ranging in thickness from 4.5 mm to 1.3 mm. Moreover, the neocortex is organized in columns which also vary in thickness and the size of their neurons. In fact, the columnar organization of the neocortex also likely played a significant role in the evolution of the neocortex (Rakic, 1995). That is, since there are numerous duplicate families of genes, most of which are silent, the activation of those "silent" (intronic) genes associated with the columnar organization of the brain could thus produce additional columns thus expanding the surface area of the neocortex. However, in this regard, as duplicate genes also exist for neurons and the laminar organization of the brain, the activation of these silent genes may also have contributed to the evolution of the neocortex, by expanding what had been three and five layered allocortex and mesocortex, into six to seven layered neocortex.
The first rudimentary forms of two to three layered cortex appears with the evolution of the lobed finned fish, and appears to have been derived from phylogenetically old, midbrain-like tissue. Over the course of evolution, these two to three layers became pushed apart such that a definite third cortical layer appeared (associated with the evolution of reptiles (Haberly 1990). In general, three layered cortex is referred to as archicortex, whereas the four to five layered cortex is referred to as mesocortex, and the six to seven layered cortex is referred to as neocortex.
Over the course of neocortical evolution, the neocortex not only expanded in thickness, adding additional layers, but it became more extensive, growing medially, laterally, caudally, and anteriorally, thus forming a smooth (lissencephalic) neocortical shroud that was grossly divisible into diffusely organized areas concerned with motor, visual, somatosensory, and auditory input (Sanides, 1970; Ulinski, 1990). Some scientists have argued that the primary motor and the primary receiving areas may have been the last neocortical areas to evolve (Sanides, 1970).
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Specifically, Sanides (1970) argues that the neocortical association areas of mammals corresponds to the limbic cortex of ancestral mammals, e.g., therapsids, and that the primary sensory and motor areas are the most recent evolutionary acquisition (Sanides, 1970). This theory is based in part of the fact that primary areas are the most heavily specialized and are almost the more elaborating developed and differentiated, whereas association areas are not as well differentiated or stratified, whereas the association areas of insectivores and monotremes is even less so. However, the problem with this theory is that monotremes, marsupials, and all other mammals possess primary receiving areas, and which resemble the primary areas of primates in regard to physiology and connectivity, and especially in regard to the intrinsic circuitry of cell columns and their cellular makeup. These features in general do not vary between species (Haug, 1987), even in regard to metabolic activity, though there are differences in the patterns of neurotransmitter innervation (Glezer et al., 1993; Hof, et al., 1992). For example, the motor areas of primates are densely innervated by DA, whereas the same is not true in regard to rats.
Other argues that the primary receiving areas and primary motor areas were the first to evolve (see Allman, 1990), and that over the course of evolution, as additional neurons and columns were generated, the primary areas began to expand and became functionally reorganized thereby forming the secondary association areas, and then the assimilation areas.
In either case, it is clear that the neocortex did expand, and it is also evident that the assimilation areas located in the anterior frontal, inferior temporal, and inferior parietal lobe, were also the last to evolve and have attained their greatest degree of development in the human brain. Indeed, the frontal lobes have expanded by almost a third over the course of the last 5 million years whereas the angular gyrus of the inferior parietal lobe probably did not fully emerge until around 50 thousand years ago (Joseph, 1999e).
As noted, in part this expansion of the neocortex appears to be due in part, to the duplication of neocortical columns and their neurons. As additional and duplicate columns were fashioned, the neocortex expanded. Since there are innumerable duplicate and uncoded copies of those genes and nucleotide sequence segments which code for the generation of these columns and their neurons (and in fact all body parts), the generation of additional columns could be accomplished quite easily once these uncoded gene segments were activated.
In addition, and as argued by Rakic (1995, p. 84) "the enlargement of existing or introduction of new cytoarchitectonic areas in evolution could occur... through... the modification of the rate and cessation of cell proliferation during" embryonic brain development. That is, since migrating neuroblasts are generated in the ventricular and subventricular zones, additional neurons can be produced if the rate of cell proliferation is increased, thereby expanding the neocortex through the additional neurons and thus additional cell columns. Again, this can be accomplished through the activation of just a few duplicate (albeit uncoded) nucleotide sequence segments that contain the necessary information for the generation of these neurons and columns.
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OVERVIEW: THE EVOLUTION OF THE MAMMALIAN NEOCORTEX
What would become the neocortex may have begun to evolve during the early stages of therapsid evolution, becoming a licencephalic neocortical shroud once the first true mammals evolved, over 100 million years ago. However, with the evolution of mammals, the neocortex continued to undergo evolutionary metamorphosis and became topograpically organized to process visual, auditory, and tactile input (Allman, 1990). The neocortex then funneled this highly processed information back to the limbic system as well as the thalamus and brainstem, creating, therefore, extensive interacting feedback loops.
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Presumably by 100 million years ago, convolutions and gyri began to form (at least in some mammals) as the neocortex began to fold up and under itself due to the limited amount of available space within the skull. The neocortex became increasingly topographically and locally organized into primary and association sensory receiving and motor expressive areas; a pattern that has since become standard among all subsequent mammalian species. Hence, the posterior regions of the hemispheres are primarily concerned with sensory perception, analysis, and association, whereas the frontal areas are concerned with motor functioning and sensory integration, regardless of species.
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Once the primary and association areas had evolved, it provided the mammals with a tremendously advanced capability to engage in multi-modal sensory analysis and information storage and thus the cognitive abilities to outthink their rivals including those "terrible lizards" the dinosaurs. In fact, by 70 million years ago, mammals were slowly gaining dominion over the planet, and throughout the world, dinosaurs were in decline. Hence, when the planet was struck by a huge meteor near the Gulf of Mexico some 65 million years ago (Alvarez, 1986; Alvarez & Asaro, 1990; Hildebrand, 1991; Raup, 1991), thus killing off almost all large sized and cold blooded land animals, the more intelligent (but smaller sized) mammals emerged comparatively unscathed whereas the remaining (smaller) and much dumber dinosaurs were simply unable to compete and were completely eradicated from the face of the planet. The age of mammals had begun, and soon humans would come to rule the Earth.
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