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Joseph, R. (1992) The Limbic System: Emotion, Laterality, and Unconscious Mind. The Psychoanalytic Review, 79, 405-456. 1992).
Emotion, Laterality, and Unconscious Mind,
Many members of Western civilization experience emotion as a potentially
overwhelming force that warrants and yet resists control - as something
irrational that can happen to you ("you make me so angry"). Perhaps in part,
this schism between the rational and the emotional is attributable to the
raw energy of emotion having its source in the nuclei of the ancient limbic
lobe - what some have referred to as the reptilian brain, a series of nuclei
that first made their phylogenetic appearance long before man walked upon
this earth. Although over the course of evolution a new brain (neocortex)
has developed, we remain creatures of emotion. We have not completely
emerged from the phylogenetic swamps of our original psychic existence. The
old limbic brain has not been replaced.
Buried within the depths of the cerebrum are several large aggregates of
limbic neurons that are preeminent in the mediation and expression of
emotional, motivational, sexual, and social behavior and that control and
monitor internal homeostasis and basic needs, such as hunger and thirst.
These regions include the hypothalamus, amygdala, hippocampus, septal
nuclei, cingulated, various thalamic nuclei, portions of the reticular
activating system, the orbital frontal lobes, certain nuclei of the
cerebellum, and other structures that together form the limbic system.
Of specific concern in this chapter are the hypothalamus, amygdala,
hippocampus, and septal nuclei, the social - emotional and psychic functions
they mediate, and the neural circuitry that supports their activity. Limbic
laterality, temporal lobe epilepsy, hallucinations and memory, and select
aspects of psychological and unconscious development, including the pleasure
principle and primary process, are also briefly discussed.
AFFECTIVE ORIGINS: OLFACTION AND SOMESTHESIS
Emotionality serves a protective function, either to promote survival of
the individual (e.g., fight or flight) of that of the species (e.g., sexual
activity). The first and most primitive manifestations of emotion are
elicited in response to olfactory (e.g., pheromones and other externally
secreted chemical messengers) and tactile sensory stimulation. These
primitive emotions are expressed as withdrawal (fear) or approach reactions
to pain or threat and are elicited in response to motivational needs, such
as the seeking of a sexual partner or for the procurement of food (prey) and
nourishment (Graeber, 1980; Michael & Keverne, 1974; Savage, 1980; Wilson,
1962).
Olfaction was originally crucial to evolutionary and phylogenetic
development, as it informed the organism about the environment at a
distance, without the necessity of physical contact. By means of olfactory
cues and the detection of pheromones, the organism is able to detect and
track food, determine the intent and social - emotional status of
conspecies, as well as signal its own intent, motivation, social position,
and/or sexual availability (Michael & Keverne, 1974; Wilson, 1962).
For example, consider pheromones, substances secreted by the skin through
specialized glands or found in urine and feces. Chemical communication
through pheromones is used by moths, social insects, dogs, cats, and
primates, as well as amphibian, sharks, and reptiles. Although detection of
pheromones among insects is often accomplished through specialized
chemoreceptors located on various parts of the body (Wilson, 1962), mammals
and pirates rely on olfactory receptors within the nostrils that transmit
this information to the olfactory bulb (or lobe in some species) and the
telencephalon (Graeber, 1980; Savage, 1980).
Among mammals, olfactory cues are also used for marking possessions and
one's territory. For example, dogs will urinate on trees and bushes, whereas
a stallion might urinate on the feces of his mare. Prosimian primates will
actually urinate on their hands, rub the secretions over their body, and
thus mark everything they come into contact with. It has also been shown
that male primates, as well as other mammals, rendered anosmic (through the
cutting of the olfactory nerves) completely lose interest in sexually
available females because of the inability to detect olfactory (pheromone)
cues indicating sexual readiness (Michael & Kaverne, 1974). Thus, olfaction
is a crucial mode of communication; among some species, the olfactory bulb
is so highly developed that it is considered a lobe of the brain.
Among humans olfaction appears to have lost its leading role in signaling
motivationally significant information. However, olfactory cues are still
employed for indicating sexuality (e.g., perfume), and odor exerts a
powerful influence on what is considered socially acceptable, hence the
abundance of artificial chemicals designed to eliminate various body
fragrances. Moreover, one need only suffer a severe cold to appreciate the
dominant function of smell in the ability to detect and appreciate fully the
flavor of food and thereby experience pleasure in eating (Fig 19). Odors
also affect learning and memory and have the capability of triggering vivid
recollections of some far away and past event.
Ontogenetically, although influenced by olfactory cues, humans first
experience or express emotionally in relationship to the body and in
response to tactile sensations or rapid changes in position (Emde & Koenig,
1969; Spitz & Wolf, 1946). Pain is also first experienced in relationship to
the body, and is somesthetically rooted, although some have argued that pain
is not an emotion.
Among human infants, the earliest smiles are induced through tactile
stimulation (e.g., light stroking or even blowing on the skin), whereas loss
of support is the most powerful stimulus for triggering an emotional
reaction in the newborn (Emde & Koenig, 1969; Sptiz & Wolf, 1946). The
earliest and most consistent manifestation of emotion in the infant consists
of screaming and crying, whereas positive affect is limited to an attitude
of acceptance and quiescence (Sptiz & Wolf, 1946), emotions first mediated
by the hypothalamus that may or may not be true emotions at all.
In their journey from the external to the internal environment, olfactory
and tactile input are transmitted to various limbic nuclei, such as the
lateral hypothalamus and entorhinal area of the hippocampus (olfactory only)
and the amygdala (olfaction and somesthesis). Indeed, it is through nuclei
such as the amygdala (as opposed to the hypothalamus) that the first true
(or rather, felt) aspects of emotion appear to be generated. It is also
because of the tremendous input of olfactory information to various limbic
nuclei that this part of the brain was at one time referred to as the
rhinencephalon, literally "nose brain."
HYPOTHALAMUS
The hypothalamus is a very ancient structure. Unlike most other brain
regions, it has maintained a striking similarity in structure throughout
phylogeny and apparently over the course of evolution (Crosby, DeJonge, &
Schneider, 1966). Located in the most medial aspect of the brain, along the
walls and floor of the third ventricle, this nucleus is fully functional at
birth and is the central core from which all emotions derive their motive
force.
The hypothalamus is highly involved in all aspects of endocrine, hormonal,
visceral, and autonomic functions; it mediates or exerts controlling
influences on eating, drinking, the experience of pleasure, rage, and
aversion. The hypothalamus is also sexually dimorphic; i.e., both
structurally and functionally, the hypothalamus of men and women is sexually
dissimilar.
Sexual Dimorphism in the Hypothalamus
As is well known, sexual differentiation is strongly influenced by the
presence or absence of gonadal steroid hormones during certain critical
periods of prenatal development in many species, including humans. However,
not only are the external genitalia and other physical features sexually
differentiated, but certain regions of the brain have also been found to be
sexually dimorphic and differentially sensitive to steroids, particularly
the preoptic area and ventromedial nucleus of the hypothalamus, as well as
the amygdala (Bleier, Byne, & Siggelkow, 1982; Dorner, 1976; Gorski, Gordon,
Shyrne, & Southam, 1978; Rainbow, Parsons, & McEwen, 1982; Raisman & Field,
1971, 1973).
Specifically, the presence or absence of the male hormone testosterone,
during this critical neonatal period, directly affects and determines the
pattern of interconnections between the amygdala and hypothalamus and
between axons and dendrities in these nuclei, and thereby the organization
of specific neural circuits. In the absence of testosterone, the female
pattern of neuronal development occurs.
For example, if the tests are removed before differentiation, or if a
chemical blocker of testosterone is administered, preventing this hormone
from reaching target cells in the limbic system, not only does the female
pattern of neuronal development occur, but makes so treated behave and
process information in a manner similar to that of females (e.g., Joseph,
Hess, & Birecree, 1978); i.e., they develop female brains. Conversely, if
females are administered testosterone during this critical period, the male
pattern of differentiation and behavior results.
That the preoptic and other hypothalamic regions are sexually dimorphic is
not surprising, in that it has long been known that this area is critical in
controlling the basal output of gonadotropins in females before ovulation
and is heavily involved in mediating cyclic changes in hormone levels, such
as follicle-stimulating estrogen, hormone (FSH), luteinizing hormone (LH),
and progesterone. Chemical and electrical stimulation of the preoptic and
ventromedial thalamic nuclei also triggers sexual behavior and even sexual
posturing in females and males (Lisk, 1967, 1971).
In primates, electrical simulation of the preoptic area increases sexual
behavior in males and significantly increases the frequency of erections,
copulations, and ejaculations, we well as pelvic thrusting followed by an
explosive discharge of semen even in the absence of a mate (Maclean, 1973).
Conversely, lesions to the preoptic and posterior hypothalamus eliminates
male sexual behavior and results in gonadal atrophy.
Lateral and Ventromedial Hypothalamic Nuclei
Although consisting of several nuclear subgroups, the lateral and medial
(ventromedial) hypothalamic nuclei play particularly important roles in the
control of the autonomic nervous system, the experience of pleasure and
aversion, eating and drinking, and raw (undirected) emotionality. These
nuclei also appear to share a somewhat antagonistic relationship (fig. 20).
For example, the medial hypothalamus controls parasympathetic activities
(e.g., reduction in heart rate, increased peripheral circulation) and exerts
a dampening effect on certain forms of emotional/motivational arousal. The
lateral hypothalamus mediates sympathetic activity (increasing heart rate,
elevating blood pressure) and is involved in controlling the metabolic and
somatic correlates of heightened emotionality. In this regard, the lateral
and medial region act to exert counterbalancing influences on each other.
Hunger and Thirst
The lateral and medial region are highly involved in monitoring internal
homeostasis and motivating the organism to respond to internal needs such as
hunger and thirst. For example, both nuclei appear to contain receptors that
are sensitive to the body's fat content (lipostatic receptors) and to
circulating metabolites (e.g., glucose), which together indicate the need
for food and nourishment. The lateral hypothalamus also appears to contain
osmoreceptors (Joynt, 1966) that determine whether water intake should be
altered.
Electrophysiologically , it has been determined that the hypothalamus not
only becomes highly active immediately before and while the organism is
eating or drinking, but the lateral region alters its activity when the
subject is hungry and is simply looking at food (Hamburg, 1971; Rolls,
Burton, and Mora, 1976). In fact, if the lateral hypothalamus is
electrically stimulated, a compulsion to eat and drink results (Delgado &
Anand, 1953). Conversely, if the lateral area is destroyed bilaterally,
aphagia and adipsia are so severe that animals will die unless force fed
(Teitelbaum & Epstein, 1962).
If the medial hypothalamus is surgically destroyed, inhibitory influences
on the lateral region appear to be abolished such that hypothalamic
hyperphagia and severe obesity result (Teitelbaum, 1961). Thus, the medial
area seems to act as a satiety center but as a center that can be
overridden.
Overall, it appears that the lateral hypothalamus is involved in the
initiation of eating and acts to maintain a lower weight limit such that
when the limit is reached the organism is stimulated to eat. Conversely, the
medial regions seems to be involved in setting a higher weight limit such
that when these levels are approached, it triggers the cessation of eating.
In part, these nuclei exert these differential influences on eating and
drinking by means of motivational/emotional influences they exert on other
brain nuclei (e.g., by reward or punishment).
Pleasure and Reward
In 1952, Heath (cited by Maclean, 1969) reported what was then considered
remarkable. Electrical stimulation near the septal nuclei elicited feelings
of pleasure in human subjects: "I have a glowing feeling. I feel good!"
Subsequently, Olds and Milner (1954) reported that rats would tirelessly
perform operants to receive electrical stimulation in this same region and
concluded that stimulation "has an effect that is apparently equivalent to
that of a conventional primary reward." Even hungry animals would
demonstrate a preference for self-stimulation over food.
Feelings of pleasure (as demonstrated by self-stimulation) have been
obtained following excitation to a number of diverse limbic areas, including
the olfactory bulbs, amygdala, hippocampus, cingulated, substantia nigra ( a
major source of dopamine), locus coeruleus (a major source of
norepinephrine), raphe nucleus (serotonin), caudate, putamen, thalamus,
reticular formation, medial forebrain bundle, and orbital frontal lobes
(Brady, 1960; Lilly, 1960; Olds & Forbes, 1981; Stein & Ray, 1959;
Waraczynski & Stellar, 1987).
In mapping the brain for positive loci for self-stimulation, Olds (1956)
found that the medial forebrain bundle (MFB) was a major pathway that
supported this activity. Although the MFB interconnects the hippocampus,
hypothalamus, septum, amygdala, and orbital frontal lobes (areas that give
rise to self-stimulation), Olds discovered that in its course up to the
lateral hypothalamus, reward sites become more densely packed. Moreover, the
greatest area of concentration and the highest rates of self-stimulatory
activity were found to occur not in the MFB but in the lateral hypothalamus
(Olds, 1956; Olds & Forbes, 1981). Indeed, animals "would continue to
stimulate as rapidly as possible until physical fatigue forced them to slow
or to sleep" (Olds, 1956).
Electrophysiological studies of a single lateral hypothalamic neurons have
also indicated that these cells become highly active in response to
rewarding food items (Nakamura & Ono, 1986). In fact, many of these cells
will become aroused by neutral stimuli repeatedly associated with rewards
such as a cue tone - even in the absence of the actual reward (Nakamura &
Ono, 1986; Nishino, Sasaki, Fukuda, & Muramoto, 1980). However, this ability
to form associations appears to be secondary to amygdaloid and other source
of input (Fukuda, Ono, & Nakamura, 1987).
Nevertheless, if the lateral region is destroyed, the experience of
pleasure and emotional responsiveness is almost completely attenuated. For
example, in primates, faces become blank and expressionless, whereas of the
lesion is unilateral, marked neglect and indifference regarding all sensory
events occurring on the contralateral side occur (Marshall & Teitelbaum,
1974). Animals will in fact cease to eat and will die.
Aversion
In contrast to the lateral hypothalamus and its involvement in pleasurable
self-stimulation, activation of the medial hypothalamus is apparently so
aversive that subjects will work to reduce it (Olds & Forbes, 1981). Thus,
electrical stimulation of the medial region leads to behavior that
terminates the stimulation - apparently so as to obtain relief (e.g., active
avoidance). In this regard, when considering behavior such as eating, it
might be postulated that when the upper weight limits (or nutritional
requirements) are met, the medial region becomes activated, which in turn
leads to behavior (e.g., cessation of eating) that terminates its
activation.
It is possible, however, that medial hypothalamic activity may also lead to
a state of quiescence such that the organism is motivated simply to cease to
respond. In some instances, this quiescent state may be physiologically
neutral, whereas in other situations the result may be highly aversive.
Nevertheless, quiescence is associated with parasympathetic activity, which
is also mediated by the medial area.
Hypothalamic Damage and Emotional Incontinence: Laughter and Rage
When electrically stimulated, the hypothalamus responds by triggering two
seemingly oppositional feeling states: pleasure and unpleasure/aversion. The
generation of these emotional reactions in turn influences the organism to
respond so as to increase or decrease what is being experienced. Through its
rich interconnections with other limbic regions, including the neocortex and
frontal lobes, the hypothalamus is able to mobilize and motivate the
organism either to cease or to continue to behave. Nevertheless, at the
level of the hypothalamus, the emotional states elicited are very primitive,
diffuse, undirected and unrefined. The organism feels pleasure in general,
or aversion/unpleasure in general. Higher-order emotional reactions (e.g.,
desire, love, hate) require the involvement of other limbic regions as well
as neocortical participation.
Emotional functioning at the level of the hypothalamus is not only quite
limited and primitive, it is also largely reflexive. For example, when
induced by stimulation, the moment the electrical stimulus is turned off,
the emotion elicited is immediately abolished. By contrast, true emotions
(which require other limbic interactions) are not simply turned on or off
but can last from minutes to hours to days and weeks before completely
dissipating.
Nevertheless, in humans, disturbances of hypothalamic functioning (e.g.,
caused by an irritating lesion such as tumor) can give rise to seemingly
complex, higher-order behavioral - emotional reactions, such as pathological
uncontrollable laughter and crying. However, in some cases, when patients
are questioned, they may deny having any feelings that correspond to emotion
displayed (Davison & Kelman, 1939; Ironside, 1956; Martin, 1950). In part,
these reactions are sometimes due to disinhibitory release of brainstem
structures involved in respiration, whereas in other instances the resulting
behavior is caused by hypothalamic triggering of other limbic nuclei.
Uncontrolled Laughter
Pathological laughter has frequently been reported to occur with
hypophyseal and midline tumors involving the hypothalamus, aneurysm in this
vicinity, hemorrhage, astrocytoma, or papilloma of the third ventricle
(resulting in hypothalamic compression), as well as surgical manipulation of
this nucleus (Davison & Kelman, 1939; Dott, 1938; Foerster & Gagel, 1933;
Martin, 1950; Money & Hosta, 1967; Ironside, 1956; List, Downman, & Bagheiv,
1958).
For example, Martin (1950) describes a man who, while "attending his
mother's funeral was seized at the graveside with an attack of
uncontrollable laughter which embarrassed and distressed him considerably"
(p. 455). Although this particular attack dissipated, it was soon
accompanied by several further fits of laughter and he died soon thereafter.
At postmortem examination, a large ruptured aneurysm was found compressing
the mamillary bodies and hypothalamus.
In a similar case (Anderson, 1936, cited by Martin, 1950), a patient
literally died laughing following eruption of the posterior communicating
artery that resulted in compression (by hemorrhage) of the hypothalamus.
"She was shaken by laughter and could not stop: short expirations followed
each other in spasms, without the patient being able to make an adequate
inspiration of air, she became cyanosed and nothing could stop the spasm of
laughter which eventually became noiseless and little more than a grimace.
After 24 hours of profound coma, she died."
Because laughter in these instances has not been accompanied by
corresponding feeling states, this pseudoemotional condition has been
referred to as sham mirth (Martin, 1950). However, in some cases, abnormal
stimulation in this region (such as due to compression effects from
neoplasm) has triggered corresponding emotions and behaviors - presumably
due to activation of other limbic nuclei.
For example, laughter has been noted to occur with hilarious or obscene
speech - usually as a prelude to stupor or death - in cases in which tumor
has infiltrated the hypothalamus (Ironside, 1956). In several instances, it
has been reported by one group of neurosurgeons (Foerster & Gagel, 1933)
that while swabbing the blood from the floor of the third ventricle,
patients "became lively, talkative, joking, and whistling each time the
infundibular region of the hypothalamus was manipulated." In one case, the
patient became excited and began to sing.
Hypothalamic Rage
Stimulation of the lateral hypothalamus can induce extremes in
emotionality, including intense attacks of rage accompanied by biting and
attack upon any moving object (Flynn, Edwards, & Bandler, 1971; Gunne &
Lewander, 1966; Wasman & Flynn, 1962). If this nucleus is destroyed,
aggressive and attack behavior is abolished (Karli & Vergness, 1969). Thus,
the lateral hypothalamus is responsible for rage and for aggressive
behavior.
The lateral hypothalamus maintains an oppositional relationship with the
medial hypothalamus. Thus, stimulation of the medial region counters the
lateral area such that rage reactions are reduced or eliminated (Ingram,
1952; Wheatley, 1944), whereas if the medial is destroyed. There results
lateral hypothalamic release and the triggering of extreme savagery.
In man, inflammation, neoplasm, and compression of the hypothalamus have
also been noted to give rise to rage attacks (Pilleri & Poeck, 1965), and
surgical manipulations or tumors within the hypothalamus have been observed
to elicit manic and ragelike outbursts (Alpers, 1940). These appear to be
release phenomenon, however. That is, rage, attack, aggressive, and related
behaviors associated with the hypothalamus appears to be under the
inhibitory influence of higher order limbic nuclei such as the amygdala and
septum (Siegel & Skog, 1970). When the controlling pathways between these
areas are damaged (i.e., disconnection) these behaviors are sometimes
elicited.
For example, Pilleri and Poeck (1965) described a man with severe damage
throughout the cerebrum, including the amygdala, hippocampus, and cingulate,
but with complete sparing of the hypothalamus, who continually reacted with
howling, growling, and baring of teeth in response to noise or a slight
touch or if approached. Hence, the hypothalamus, being released, responds
reflexively in an aggressive nonspecific manner to any stimulus. Lesions of
the frontal - hypothalamic pathways have been noted to result in severe rage
reactions as well (Fulton & Ingraham, 1929; Kennard, 1945).
Nevertheless, like sham mirth, rage reactions elicited in response to
direct electrical activation of the hypothalamus immediately and completely
dissipate when the stimulation is removed. These outbursts have been
referred to as sham rage.
Lateralization
Although scant, there is some evidence to suggest that the right
hypothalamus may be more heavily involved in the control of neuroendocrine
functioning, particularly in females. Greater right hypothalamic
concentration of substancessuch as LHRH (luteinizing hormone) has also been
reported (see Gerendai, 1984, for review).
Psychic Manifestations of Hypothalamic Acitivity
Phylogenetically and from an evolutionary perspective, the appearance and
development of the hypothalamus predate the emergence and differentiation of
all other limbic nuclei, e.g., amygdala, septal nucleus, and hippocampus
(Andy & Stephen, 1961; Brown, 1983; Herrick, 1925; Humphrey, 1972). It
constitutes the most primitive, archaic, reflexive, and purely biological
aspect of the psyche.
Biologically, the hypothalamus serves the body tissues by attempting to
maintain internal homeostasis and by providing for the immediate discharge
of tenions in an almost reflexive manner. Studies of lateral and medial
hypothalamic functioning indicate that it appears to act reflexively, in an
almost on/off manner so as to seek or maintain the experience of pleasure
and escape or avoid unpleasant noxious conditions.
Emotions elicited by the hypothalamus are largely undirected, short-lived,
and unconnected with events occurring within the external environment, being
triggered reflexively and without concern or understanding regarding
consequences. Direct contact with the real world is quite limited and almost
entirely indirect as the hypothalamus is largely concerned with the internal
environment of the organism. It has no sense of morals, danger, values,
logic, and so forth, and can neither feel nor express love or hate. Although
quite powerful, hypothalamic emotions are largely undifferentiated,
consisting of such feelings as pleasure, unpleasure, aversion, rage, hunger,
and thirst.
As the hypothalamus is concerned with the internal environment, much of its
activity occurs outside conscious-awareness. Moreover, being involved in
maintaining internal homeostasis, through, for example, its ability to
reward or punish the organism with feelings of pleasure or aversion, it
tends to serve what Freud (1911) described as the pleasure principle.
The Pleasure Principle
The lateral and medial nuclei exert counterbalancing influences that serve
to modulate activity occurring in the other. As described by Freud (1911),
the pleasure principle not only serves to maximize pleasant experiences, but
acts to keep the psyche as a whole free from high levels of excitation (be
they pleasurable or unpleasant).
Like the hypothalamus, the pleasure principle is present from birth and for
some time thereafter the search for pleasure is manifested in an
unrestricted manner and with great intensity, as there are no oppositional
forces (except those between the lateral and medial regions) to counter it's
strivings. Indeed, higher order limbic nuclei have yet to mature.
Functionally isolated, the hypothalamus at birth has no way of reducing
tension or of mobilizing the organism for any form of effective action. It
is helpless. When tensions associated with immediate needs (e.g., hunger or
thirst) become unpleasant the only response available to the hypothalamus is
to cry and make ragelike vocalizations. When satiated, the hypothalamus can
only respond with a feeling state suggesting pleasure or at least
quiescence. Indeed, as is well known, for the first few months of life, the
infant's awareness largely consists of a very restricted matrix involving
tactile, visceral (hunger), and kinesthetic sensations, whereas emotionally
the infant is capable of screaming, crying, or demonstrating very
rudimentary features of pleasure, i.e., an attitude of acceptance of
quiescence (McGraw, 1969; Milner, 1967; Piaget, 1952; Spitz & Wolf, 1946).
It is only with the further differentiation and maturation of higher-order
limbic nuclei (e.g., amygdala, septal nucleus, hippocampus) that the infant
begins to achieve some awareness of external reality and begins to form
memories as well as differentiate and associate externally occurring events
and individuals.
AMYGDALA
In contrast to the primitive hypothalamus, the more recently developed
amygdala is preeminent in the control and mediation of all higher order
emotional and motivational activities. Through its rich interconnections
with various neocortical and subcortical regions, amygdaloid neurons are
able to monitor and abstract from the sensory array stimuli that are of
motivational significance to the organism (Steklis & Kling, 1985). This
includes the ability to discern and express even subtle social - emotional
nuances such as friendliness, fear, love, affection, distrust, and anger,
and at a more basic level, determine whether something might be good to eat.
In fact, amygdaloid neurons respond selectively to the flavor of certain
preferred foods, as well as to the sight or sound of something that might be
especially desirable to eat (Fukuda et al., 1987; O'Keefe & Bouma, 1969; Ono
et al., 1980).
Single amygdaloid neurons receive considerable topographic input, and are
predominantly polymodal, responding to a variety of stimuli from different
modalities simultaneously (O'Keefe & Bouma, 1969; Perryman, Kling, & Lloyd,
1987; Sawa & Delgado, 1963; Schutze, Knuepfer, Eismann, Stumpf, & Stock,
1987; Turner, Mishkin, & Knapp, 1980; Ursin & Kaasa, 1960; Van Hoesen,
1981). The amygdala is also very sensitive to somesthetic input and physical
contact such that even a slight touch in a very circumscribed area of the
body can produce amygdaloid excitation. Overall, in addition to emotional
and motivational functioning, because multimodal assimilation of various
sensory impressions occurs in this region, it is also involved in attention,
learning, and memory.
Medial and Lateral Amygdaloid Nuclei
The amygdala is buried within the depths of the anterior - inferior temporal
lobe and consists of two major nuclear groups. These are a phylogenetically
ancient anteromedial group (or medial amygdala) involved in olfaction and
motor activity, as well as a relatively newer basolateral division (lateral
amygdala) that first appears in primates (Herrick, 1925; Humphrey, 1972).
Like the lateral and medial hypothalamus, these two amygdaloid nuclei
subserve different functions and maintain different anatomical
interconnections.
Emybryologically, the medial amygdala is the first portion of the basal
ganglia striatal complex to appear during development, being formed through
neuroblast migration from the epithilium of the lateral ventricle (Humphrey,
1972). As it circles in an arc from the frontal to temporal lobe, the tail
of the caudate nucleus actually terminates and merges with the amygdala.
This portion of the amygdala is in fact part of the basal ganglia and is
heavily involved in motivating and coordinating gross, or whole-body, motor
activity.
The medial amygdala receives fibers from the olfactory tract and through a
rope of fibers called the stria terminalis, projects directly to and
receives fibers from the medial hypothalamus (through which it exerts
inhibitory influences) as well as the septal nucleus (Carlsen, De Olmos, &
Heimer, 1982; Gloor, 1955; Russchen, 1982; Swanson & Cowan, 1979). In
addition, the medial (and lateral) regions are rich in cells containing
enkephalins, and opiate receptors can be found throughout the amygdala
(Atweh & Kuhar, 1977; Uhl, Kudar, & Snyder, 1978).
Sexuality
Portions of the hypothalamus and amygdala are sexually dimorphic; i.e.,
there are male and female amygdaloid nuclei. Thus, at a very basic and
primitive level, emotional and motivational perceptual/behavioral
functioning becomes influenced and guided by the neuroanatomical sexual bias
of the host. Electrical stimulation of the amygdala, the medial division in
particular, results in sex-related behavior and activity. In females this
includes ovulation, uterine contractions and lactogenetic responses, and in
males penile erections (Robinson & Mishkin, 1968; Shealy & Peele, 1957).
Damage to the amygdala bilaterally often results in heightened and
indiscriminant sexual activity. For example, primates and other animals
(while in captivity) will engage in excessive masturbation and genital
manipulation and will repeatedly attempt to copulate even with species other
than their own (e.g., a cat with a dog, a dog with a turtle) regardless of
their sex. With bilateral destruction, animals are not only overly active
sexually but are able to identify appropriate partners (Brown & Schaefer,
1888; Kluver & Bucy, 1939). This abnormality is one aspect of a complex of
symptoms sometimes referred to as the Kluver - Bucy syndrome (to be
discussed in more detail below).
Lateral Amygdala
With the evolutionary ascent of primates, the relatively new lateral
division of the amygdala progressively expands and differentiates. The
lateral amygdala contributes fibers to the stria terminalis and gives rise
to the amygdalofugal pathway, through which it projects to the lateral and
medial hypothalamus (upon which it exerts inhibitory and excitatory
influences, respectively), the dorsal medial thalamus (which is involved in
memory, attention, and arousal), olfactory tubercle, as well as other
subcortical regions (Aggleton, Burton, & Passingham, 1980; Carlsen, et al.,
1982; Dreifuss et al., 1968; Gloor, 1955, 1960; Klinger & Gloor, 1960;
Mehler, 1980; Russchen, 1982). It also receives fibers from the medial
forebrain bundle, which in turn has its site of origin in the lateral
hypothalamus (Mehler, 1980).
In general, whereas the medial amygdala is highly involved in motor,
olfactory and sexual functioning, the lateral division is intimately
involved in all aspects of higher order emotional activity; hence its rich
interconnections with the lateral and medial hypothalamus, and the
neocortex. The lateral amygdala maintains rich interconnections with the
inferior, middle, and superior temporal lobes, as well as the insular
temporal region, which in turn allows it to sample and influence the
auditory, somesthetic, and visual information being received and processed
in these areas, as well as to scrutinize this information for motivational
and emotional significance (Herzog & Van Hoesen, 1976; Kling et al., 1987;
Machne & Segundo, 1956; Mesulam & Mufson, 1982; O'Keefe & Bouma, 1969;
Steklis & Kling, 1985; Turner et al., 1980; Van Hoesen, 1981). Gustatory and
respiratory sense are also rerepresented in this vicinity (Fukuda et al.,
1987; Maclean, 1949; Ono et al., 1980), and the lateral division maintains
rich interconnections with cingulated gyrus, orbital frontal lobes (Pandya,
Van Hoesen, Domeskick, 1973), and the parietal cortex (O'Keefe & Bouma,
1969), through which it receives complex somesthetic information.
The lateral amygdala is highly important in analyzing information received
and transferring information back to the neocortex so that further
elaboration may be carried out at the cortical level. It is through the
lateral division that emotional meaning and significance can be assigned to
as well as extracted from that which is experienced.
The amygdala, overall, maintains a functionally interdependent relationship
with the hypothalamus. It is able to modulate and even control rudimentary
emotional forces governed by the hypothalamic nucleus. However, it also acts
at the behest of hypothalamically induced drives. For example, if certain
nutritional requirements need to be met, the hypothalamus signals the
amygdala, which then surveys the external environment for something good to
eat. By contrast, when, via environmental surveilance, the amygdala
discovers a potentially threatening stimulus, it acts to excite and drive
the hypothalamus so that the organism is mobilized to take appropriate
action. Thus, when the hypothalamus is activated by the amygdala, instead of
responding in an on - off manner, cellular activity continues for an
appreciably longer time period (Dreifuss et al., 1968). The amygdala can tap
into the reservoir of emotional energy mediated by the hypothalamus to
achieve certain ends.
Attention
The amygdala acts to perform environmental surveillance and can trigger
orienting responses as well as mediate the maintenance of attention if
something of interest or importance were to appear (Gloor, 1955, 1960;
Kaada, 1951; Ursin & Kaasa, 1960). Electrical stimulation of the lateral
division can initiate quick and/or anxious glancing and searching movements
of the eyes and head, such that the organism appears aroused and highly
alert as if in expectation of something that is going to happen (Ursin &
Kaada, 1960). The EEG becomes desynchronized (indicating arousal), heart
rate becomes depressed, respiration patterns change, and the galvanic skin
response significantly alters (Bagshaw & Benzies, 1968; Ursin & Kaada, 1960)
- reactions that characteristically accompany the orienting response of most
species. Once a stimulus of potential interest is detected, the amygdala
acts to analyze its emotional - motivational importance and will act to
alert other nuclei such as the hypothalamus so that appropriate action may
take place.
Fear, Rage, and Aggression
Initially, electrical stimulation of the amygdala produces sustained
attention and orienting reactions. If the stimulation continues fear and/or
rage reactions are elicited (Ursin & Kaada, 1960). When fear follows the
attention response, the pupils dilate and the subject will cringe, withdraw,
and cower. This cowering reaction in turn may give way to extreme fear
and/or panic such that the animal will attempt to take flight.
Among humans, the fear response is one of the most common manifestations of
amygdaloid electrical stimulation. Moreover, unlike hypothalamic on/off
emotional reactions, attention and fear reactions can last up to several
minutes after the withdrawal of stimulation.
In addition to behavioral manifestations of heightened emotionality,
amygdaloid stimulation can result in intense changes in emotional facial
expression. This includes facial contortions, baring of the teeth, dilation
of the pupils, widening or narrowing of the eyelids, flaring of the
nostrils, tearing, as well as sniffing, licking, and chewing (Anand & Dua,
1955; Ursin & Kaada, 1960). Indeed, some of the behavioral manifestations of
a seizure in this vicinity (i.e., temporal lobe epilepsy) typically include
chewing, smacking of the lips, and licking.
In many instances, rather than fear, there instead results anger,
irritation, and rage, which seems to build up gradually, until finally the
animal or human attacks (Egger & Flynn, 1963; Gunne & Lewander, 1966; Ursin
& Kaada, 1960; Zbrozyna, 1963). Unlike hypothalamic sham rage, amygdaloid
activation results in attacks directed at something real or, in the absence
of an actual stimulus, at something imaginary. Moreover, rage and attack
will persist well beyond the termination of the electrical stimulation of
the amygdala. In fact, the amygdala remains electrophysiologically active
for long periods, even after a stimulus has been removed (be it external -
perceptual, or internal - electrical), such that is appears to continue to
process - in the abstract - information even when that information is no
longer observable (O'Keefe & Bouma, 1969).
In addition to permitting sustained electrophysiological activity, the
amygdala has been shown to be heavily involved in the maintenance of
behavioral responsiveness even in the absence of an immediately tangible or
visible objective or stimulus (O'Keefe & Bouma, 1969). This includes
motivating the organism to engage in the seeking of hidden objects or
continuing a certain activity in anticipation of achieving some particular
long-term goal. At a more immediate level, the amygdala is probably very
important in object permanence (i.e., keeping an object in mind when it is
no longer visible) and concrete or abstract anticipation. Anticipation is,
of course, very important in the prolongation of emotional states such as
fear or anger, as well as the generation of more complex emotions such as
anxiety. In this regard, the amygdala is probably important not only in
regard to emotion, but in maintaining mood states.
Fear and rage reactions have also been triggered in humans following depth
electrode stimulation of the amygdala (Chapman, 1960; Chapman, Schroeder,
Geyer, Brazier, Fager, Poppen, Solomoan, & Yakovlev, 1954; Heath, Monroe, &
Mickle, 1955; Mark, Ervin, & Sweet, 1972). Mark et al. (1972) describe one
female patient who following amygdaloid stimulation became irritable and
angry, and then enraged. Her lips retracted, there was extreme facial
grimacing, threatening behavior, and then rage and attack - all of which
persisted well beyond stimulus termination.
Similarly, Schiff et al. (1982) described a man who developed intractable
aggression following a head injury and damage (determined via depth
electrode) to the amygdala (i.e., abnormal electrical activity).
Subsequently, he became easily enraged, sexually preoccupied (although
sexually hypoactive), and developed hyperreligiosity and psuedomystical
ideas. Tumors invading the amygdala have been reported to trigger rage
attacks (Sweet, Ervin, & Mark, 1960; Vonderache, 1940).
The amygdala appears capable of not only triggering and steering
hypothalamic activity but acting on higher level neocortical processes so
that individuals form emotional ideas. Indeed, the amygdale is able to
overwhelm the neocortex and the rest of the brain so that the person not
only forms emotional ideas but responds to them. A famous example of this is
Charles Whitman, who in 1966 climbed a tower at the University of Texas and
began to indiscriminantly kill people with a rifle.
Whitman had initially consulted a psychiatrist about his periodic and
uncontrollable violent impulses but was unable to obtain relief. Prior to
climbing the tower, he wrote himself a letter (Sweet et al., 1969):
I don't really understand myself these days. Lately I have been a victim of
many unusual and irrational thoughts. These thoughts constantly recur, and
it requires a tremendous mental effort to concentrate. I talked to a doctor
once for about two hours and tried to convey to him my fears that I felt
overcome by overwhelming violent impulses. After one session I never saw the
Doctor again, and since then I have been fighting my mental turmoil alone.
After my death I wish that an autopsy would be performed to see if there is
any visible physical disorder. I have had tremendous headaches in the past.
Later he wrote:
It was after much thought that I decided to kill my wife, Kathy, tonight
after I pick her up from work....I love her dearly, and she has been a fine
wife to me as any man could ever hope to have. I cannot rationally pinpoint
any specific reason for doing this....
That evening, he killed his wife and mother and wrote:
I imagine that it appears that I brutally killed both of my loved ones. I
was only trying to do a good thorough job....
The following morning, he climbed the University tower carrying a
high-powered hunting rifle and for the next 90 min he shot at everything
that moved, killing 14 and wounding 38. Postmortem autopsy of his brain
demonstrated a glioblastoma multiforme tumor the size of a walnut
compressing the amygdaloid nucleus.
Docility and Amygdaloid Destruction
Bilateral destruction of the amygdala usually results in increased
tameness, docility, and reduced aggressiveness in cats, monkeys and other
animals (Schreiner and Kling, 1956; Weiskrantz, 1956; Vochteloo & Koolhas,
1987), including purportedly ferocious creatures such as the agouti and lynx
(Schreiner and Kling, 1956). In man, bilateral amygdala destruction (by
neurosurgery) has been reported to reduce and/or eliminate paroxysmal
aggressive and violent behavior (Terzian & Ore, 1955).
In some creatures, however, bilateral ablation of the amygdala has been
reported to at least initially result in increased aggressive responding
(Bard & Mountcastle, 1948) and, if sufficiently aroused or irritated, even
the most placid of amygdalectomized animals can be induced to fight fiercely
(Fuller, Rosvold, & Pribram, 1957). However, these aggressive responses are
very short-lived and appear to be reflexively mediated by the hypothalamus.
Thus, these findings (and the data reviewed above) suggest that true
aggressive feelings are dependent on the functional integrity of the
amygdala (versus the hypothalamus).
Social - Emotional Agnosia
Among primates and mammals, bilateral destruction of the amygdala
significantly disturbs the ability to determine and identify the
motivational and emotional significance of externally occurring events, to
discern social - emotional nuances conveyed by others, or to select what
behavior is appropriate for a specific social context (Bunnel, 1966; Fuller,
Rosvold & Pribram, 1957; Gloor, 1960; Kluver & Bucy, 1939). Bilateral
lesions lower responsiveness to aversive and social stimuli, reduce
aggressiveness, fearfulness, competitiveness, dominance, and social interest
(Rosvold, Mirsky, & Pribram, 1954). Indeed, this condition is so pervasive
that subjects seem to have tremendous difficulty discerning the meaning or
recognizing the significance of even common objects - a condition sometimes
referred to as psychic blindness or the Kluver - Bucy syndrome.
Thus, animals with bilateral amygdaloid destruction, although able to see
and interact with their environment, respond in an emotionally blunted
manner and seem unable to recognize what they see, feel, and experience.
Things seem stripped of meaning. Like an infant (who similarly is without a
fully functional amygdala), patients with this condition engage in extreme
orality and will indiscriminantly pick up various objects and place them in
their mouth regardless of its appropriateness. There is a repetitive quality
to this behavior, for once they put it down they seem to have forgotten that
they had just explored it, and will immediately pick it up and place it
again in their mouth as if it were a completely unfamiliar object.
Although ostensibly exploratory, there is thus a failure to learn, to
remember, to discern motivational significance, to habituate with repeated
contact, or to discriminate between appropriate and inappropriate stimuli.
Rather, when the amygdala has been removed bilaterally, the organism reverts
to the most basic and primitive modes of object interaction such that
everything that is seen and touched is placed in the mouth (Brown &
Schaffer, 1888; Gloor, 1960; Kluver & Bucy, 1939). This condition pervades
all aspects of higher-level social - emotional functioning, including the
ability to interact appropriately with loved ones.
For example, Terzian and Ore (1955) described a young man who, following
bilateral removal of the amygdala, subsequently demonstrated an inability to
recognize anyone, including close friends, relatives, and his mother. He
ceased to respond in an emotional manner to his environment and seemed
unable to recognize feelings expressed by others. He also exhibited many
features of the Kluver - Bucy syndrome (perserverative oral "exploratory"
behavior and psychic blindness), as well as an insatiable appetite. In
addition, he became extremely socially unresponsive such that he preferred
to sit in isolation, well away from others.
Among primates who have undergone bilateral amygdaloid removal, once they
are released from captivity and allowed to return to their social group, a
social - emotional agnosia becomes readily apparent, as they no longer
respond to or seem able to appreciate or understand emotional or social
nuances. Indeed, they appear to have little or no interest in social
activity and persistently attempt to avoid contact with others (Dick, Myers,
& Kling, 1969; Jonason & Enloe, 1971; Jonason, Enloe, Contrucci, & Meyer,
1973). If approached they withdraw, and if followed they flee. Indeed, they
behave as if they have no understanding of what is expected of them or what
others intend or are attempting to convey, even when the behavior is quite
friendly and concerned. Among adults with bilateral lesions, total isolation
seems to be preferred.
In addition, they no longer display appropriate social or emotional
behaviors, and if kept in captivity will fall in dominance in a group or
competitive situation - even when formerly dominant (Bunnel, 1966; Dicks et
al., 1969; Fuller et al., 1957; Jonason & Enloe, 1971; Jonason et al., 1973;
Rosvold, Mirsky, & Pribram, 1954). As might be expected, maternal behavior
is severely affected. According to Kling (1972), mothers will behave as if
their "infant were a strange object to be mouthed, bitten, and tossed around
as though it were a rubber ball."
Laterality and the Amygdala
Limbic Language
Although language is usually discussed in regard to grammar and vocabulary,
there is a third major feature to expression and comprehension through which
a speaker may convey, and a listener determine, intent, attitude, feeling,
and meaning. Language is both descriptive and emotional. A listener
comprehends not only what is said, but how it is said - what a speaker
feels.
Feeling and attitude is generally communicated via vocal inflection,
intonation, and melody such that anger, happiness, sadness, sarcasm, and so
forth, are indicated by such cues as variations in pitch, timbre, and stress
contours - vocal capacities associated with the functional integrity of the
right cerebral hemisphere, and the right frontal and temporal regions in
particular (Joseph, 1988a; see also Chapter 1, The Right Cerebral
Hemisphere). For example, studies using dichotic listening have repeatedly
shown that the right hemisphere is superior in distinguishing stress and
pitch contours, determining frequency, amplitude, melody, duration,
processing inflectional contours, and even decoding contextual information
in the absence of denotative speech.
Conversely, patients who have undergone right temporal lobe neurosurgery or
who have suffered damage involving this area, often demonstrate impairments
in regard to many aspects of prosodic - melodic perception, such that
nonverbal environmental sounds and musical stimuli fail to be adequately
recognized. People who have suffered deep right frontal or temporal lobe
damage also have difficulty controlling the pitch and inflection of their
voice, whereas patients undergoing sodium amytal anesthetization of the
right hemisphere speak in a bland monotone.
It has been argued in detail (Joseph, 1982, 1988a) that the superior
capacity of the right hemisphere in processing and expressing melodic -
prosodic - emotional information is directly related to lateralized limbic
functioning, and in particular, a greater abundance of neuronal
interconnections with various limbic nuclei such as the amygdale. Emotional
vocalizations are limbic in origin and are hierarchically represented,
processed, and expressed by various neocortical regions within the frontal
and temporal lobes.
In fact, the major fiber pathway that links the language axis (Wernicke's
and Broca's areas) of the left hemisphere and the melodic - prosodic -
emotional Axis of the right, i.e., the arcuate fasciculus, extends from the
left frontal convexity (Broca's area) through the inferior parietal lobule,
and after giving off major fibers to Wernicke'e region continues down into
the depths of the inferior temporal lobe where it establishes contact with
the amygdala. In this way, the amygdala has a significant influence on
emotional speech (Figs. 21-23).
Indeed, both phylogenetically and ontogenetically, the original impetus to
vocalize springs forth from roots buried within the depths of the ancient
limbic lobes (e.g., amygdala, hypothalamus, septum). For example, although
nonhumans do not have the capacity to speak, they still vocalize, and these
vocalizations are primarily limbic in origin, being evoked in situations
involving sexual arousal, terror, anger, flight, helplessness, and
separation from the primary caretaker when young. The first vocalizations of
human infants are similarly emotional in origin and limbically mediated
(Joseph, 1982).
Although cries and vocalizations indicative of rage or pleasure have been
elicited through hypothalamic stimulation, of all limbic nuclei the amygdale
is the most vocally active - particularly the lateral division (Robinson,
1967). In humans and animals, a wide range of emotional sounds have been
evoked through amygdala activation, such as sounds indicative of pleasure,
sadness, happiness, and anger (Robinson, 1967; Ursin & Kaada, 1960).
Conversely, in man, destruction limited to the amygdala, (Freeman &
Williams, 1952, 1963), the right amygdala, in particular, has abolished the
ability to sing, convey melodic information, or properly enunciate by vocal
inflection. Similar disturbances occur with right hemisphere damage (Joseph,
1988a). Indeed, when the right temporal region (including the amygdala) has
been grossly damaged or surgically removed, the ability to perceive,
process, or even vocally reproduce most aspects of musical and emotional
auditory input is significantly curtailed. (See Chapter 1, The Right
Cerebral Hemisphere.)
Emotion and Temporal Lobe Seizures
The amygdala is buried within the depths of the anterior - inferior
temporal lobe and maintains rich interconnections with areas throughout the
temporal neocortex. Because of their intimate association, damage to the
temporal lobe, particularly the anterior regions, often involves and
disrupts amygdaloid functioning. In fact, because the amygdala and inferior-
anterior temporal lobe have, of all brain regions, the lowest seizure
threshold, and are minimally resistant, and are therefore maximally
vulnerable to developing abnormal seizure activity, even mild injuries may
result in kindling (i.e., abnormal activation), and therefore disruption of
their functional integrity. Indeed, damage to adjacent tissue has been known
to spread, by kindling, to the amygdala and inferior regions. Once
consequence is temporal lobe epilepsy.
Personality, emotional, and sexual disturbances are a frequent complication
of temporal lobe seizures in a significant minority of patients. Such
patients may develop paranoid, hysterical, or depressive tendencies,
deepening of mood, hyposexuality, and other characteristics suggestive of
affective disorders (Bear, Leven, Blumer, Chetam, & Ryder, 1982; Gibbs,
1951; Herman & Chambria, 1980; Strauss, Risser, & Jones, 1982; Williams,
1956). Immediately following or during the course of a seizure 10% or more
of such patients experience a change in emotionality (Herman & Chambria,
1980; Strauss et al., 1982; Williams 1956).
In part, because the highest incidence of psychiatric disorder occurs in
cases in which the EEG spike focus is in the anterior temporal area (Gibbs,
1951), and because limbic nuclei such as the amygdala are frequently
involved, it has been postulated that seizure activity sometimes
hyperactivates these nuclei (Bear, 1979), which in turn distorts the
affective meaning applied to afferent streams of visual, auditory, and
somesthetic information (Gibbs, 1951).
Thus, during a seizure, these patients may be temporarily overwhelmed by
feelings such as fear, or things they see or hear seem to become abnormally
invested with emotional significance (Bear et al., 1979; Gibbs, 1951; Gloor
et al., 1982), presumably due to abnormal amygdala activation.
Interestingly, one common symptom of temporal lobe epilepsy is an aura of
tastes, and more often odors, that are usually quite unpleasant (e.g., like
burning wire, burning feces, burning rubber or tires).
Seizure induced emotional changes tend to predominantly involve feelings of
depression, pleasure, displeasure, or fear - with fear being one of the most
common emotional experiences (Gloor et al., 1982; Williams, 1956). More
rarely, seizures involving sexual behavior, crying, laughing, or ragelike
responses have been associated with temporal lobe epilepsy.
There is some evidence to suggest that certain emotional changes are more
frequently associated with seizure originating in the right temporal lobe
and/or amygdale, whereas disturbances involving thought (e.g., psychosis,
schizophrenia) characterize left temporal lobe abnormalities (Flor-Henry,
1969, 1983; Offen, Davidoff, Troost, & Richey, 1976; Joseph, 1988; Sherwin,
1981; Schiff et al., 1982; Taylor, 1975; Weil, 1956).
For example, in their depth electrode study of five patients with seizure
disorders, Gloor et al., (1982) found that all feelings of fear and
displeasure were associated with right temporal, right amygdala, or right
hippocampal activation. These findings are consistent with the observations
of Slater, Beard, and Glithero (1969), Bear and Fedio (1977), Flor-Henry
(1969), and others, who have noted an association between right temporal
seizures and affective disorders.
Other reports, however, have been less clear cut - presumably because
seizures originating in the amygdala/temporal lobe can quickly spread from
hemisphere to another (through the anterior commissure) and because of the
failure to employ depth electrodes to pinpoint the seizure foci. Thus, in
some instances, emotions such as fear seem to arise regardless of which
hemisphere is involved (Strauss et al., 1982). Nevertheless, even in these
cases, an emotional dichotomy is apparent. For example, Herman and Chambria
(1980) described cases with right temporal foci in whom free-floating fears
developed that were not tied to something specific but that encompassed
terrifying, "death-like" and "nightmarish" feelings, whereas a patient with
a left temporal foci developed intense fears but were unable to describe
what they were afraid of.
Stimulation of the amygdala can significantly alter facial emotional
expression, including tearing. In a small minority of cases, right temporal
seizures have been reported to cause paroxysmal attacks of weeping, with
lacrimation, the making of mournful sounds, including sobbing and crying
(Offen et al., 1976). However, crying as well as laughing seizures have also
been noted to occur with left-sided involvement (Chen & Forster, 1973; Sethi
& Rao, 1976). Nevertheless, without the benefit of depth electrodes, such as
employed by Gloor and colleagues (1982), it is difficult to determine in
which amygdala and/or temporal lobe a seizure actually originates.
The amygdala and regions of the hypothalamus are sexually dimorphic, and
stimulation of either area can trigger sexual behavior. Similarly,
sensations of sexual excitement, sometimes leading to orgasm, may also occur
as a function of seizures originating in the temporal lobe (Currier, Little,
Suess, & Andy, 1971; Freemon & Nevis, 1969; Remillard et al., 1983) and in
the frontal lobe (Spencer, Spencer, Williamson, & Mattson, 1983). Of
interest, 7 of 10 patients with sexual seizures described by Remillard et
al., (1983) had foci originating in the right hemisphere. Similar findings
have been reported by Freemon & Nevis (1969), Penfield and Rasmussen (1950,
p.27), and Spencer et al. (1983).
Sexual seizures caused by temporal lobe abnormalities are often accompanied
by actual sexual behavior. "The patient was sitting at the kitchen table
with her daughter making out a shopping list. She stopped, appeared dazed,
slumped to the floor on her back, lifted her skirt, spread her knees, and
elevated her pelvis rhythmically. She made appropriate vocalizations for
sexual intercourse, such as "it feels so good" and "further, further"
(Currier et al., 1971, p.260).
Frontal Lobe Sexual Seizures
The frontal lobes, the orbital region in particular, maintain rich
interconnections with the amygdala (Nauta, 1964), and receives olfactory
projections as well (Tanabe, 1975). Epileptiform activity arising in the
deep frontal (orbital) regions has also been associated with the development
of sexual seizures, including exhibitionism, genital manipulation, and
masturbatory activity (Spencer et al., 1983).
Similar to that described regarding right temporal emotional and sexual
disturbances, Spencer et al. (1983) found that three of their four patients
with sexual automatism had seizures originating in the right frontal area,
whereas the remaining patient had bifrontal disturbances. Other
investigators have also noted that peculiar disturbances in emotion and
personality are far more likely to arise following right versus left frontal
damage (Joseph, 1986, 1988; Hillbom, 1960; Lishman, 1968).
Presumably, at least in part, emotional and sexual disturbances associated
with right temporal and right frontal (orbital) dysfunction are caused by
activation of the limbic structures, with which they intimately
interconnected. However, there is also much evidence to indicate that in
some respects, inferior temporal and orbital frontal areas are in fact
outgrowths of and thus part of the limbic system.
Summary
Over the course of early evolutionary development, the hypothalamus reigned
supreme in the control and expression of raw and reflexive emotionality,
i.e., pleasure, displeasure, aversion, and rage. Largely, however, it has
acted as an eye turned inward, monitoring internal homeostasis and concerned
with basic needs. With the development of the amygdala, the organism was now
equipped with an eye turned outward, so that the external emotional features
of reality could be tested and ascertained. When signaled by the
hypothalamus the amygdala begins to search the sensory array for appropriate
emotional - motivational stimuli, until what is desired is discovered and
attended to.
However, with the differentiation of the amygdala, emotional functioning
also became differentiated and highly refined. The amygdala hierarchically
wrested control of emotion from the hypothalamus. The amygdala is primary in
regard to the perception and expression of most aspects of emotionality,
including fear, aggression, pleasure, happiness, and sadness, and in fact
assigns emotional or motivational significance to that which is experienced.
It can thus induce the organism to act on something seen, felt, heard, or
anticipated. The integrity of the amygdala is essential in regard to the
analysis of social-emotional nuances, the organization and mobilization of
the person's internal motivational status regarding these cues, as well as
the mediation of higher-order emotional expression and impulse control. When
damaged or functionally compromised, social-emotional functioning becomes
grossly disturbed.
Through its rich interconnections with other brain regions, the amygdaloid
nucleus is able to sample and influence activity that occurs in other parts
of the cerebrum and add emotional color to one's perceptions. As such, it is
highly involved in the assimilation and association of divergent emotional,
motivational, somesthetic, visceral, auditory, visual, motor, olfactory, and
gustatory stimuli. Thus, it is very much involved with learning, memory, and
attention can generate reinforcement for certain behaviors (Douglas, 1967).
Moreover, through reward or punishment, it can promote the encoding,
storage, and later retrieval of particular types of information. That is,
learning often involves reward, and it is through the amygdala (in concert
with other nuclei) that emotional consequences can be attributed to certain
events, actions, or experiences, as well as extracted from the world of
possibility, so that it can be attended to and remembered.
Lastly, as is evident from studies of patients displaying abnormal activity
or seizures originating in or involving this nuclei, the amygdala is able to
overwhelm the neocortex and gain control over behavior. As based on
electrophysiological studies, the amygdala seems to be capable of literally
turning off the neocortex (such as occurs during a seizure), at least for
brief time periods. That is, the amygdala can induce electrophysiological
slow-wave theta activity in the neocortex, which indicates low levels of
arousal as well as high voltage fast activity. In the normal brain, it
probably exerts similar influences such that at times people (i.e., their
neocortex) lose control over themselves and respond in a highly emotionally
charged manner.
HIPPOCAMPUS
The hippocampus is an elongated structure located within the inferior
medial wall of the temporal lobe (posterior to the amygdale); it surrounds,
in part, the lateral ventricle. In humans, the hippocampus consists of an
anterior and posterior region and is shaped somewhat like a telephone
receiver.
There are three major neural pathways leading to and from the hippocampus.
These include the fornix-fimbrial fiber system, a supracallosal pathway
(i.e., the indusium griseum), which passes through the cingulated, and
through the entorhinal area, sometimes referred to as the gateway to the
hippocampus.
It is through the entorhinal area that the hippocampus receives olfactory
and amygdaloid projections (Carlsen et al., 1982; Gloor, 1955; Krettek &
Price, 1976a; Steward, 1977) and fibers from the orbital frontal and
temporal lobes (Van Hoesen et al., 1972). It is through the fornix and
fimbrial pathways that the hippocampus makes major interconnections with the
thalamus, septal nuclei, medial hypothalamus, and through which it exerts
either inhibitory or excitatory influences on these nuclei (Feldman,
Saphier, & Conforti, 1987; Guillary, 1957; Poletti & Sujatanon, 1980).
Septal interactions: The hippocampus maintains a particularly intimate
relationship with the septal nuclei (sometimes referred to as the septum -
not to be confused with the septum pelucidum). The septal nucleus partly
serves as in interactional relay center as it channels hippocampal
influences to other structures such as the hypothalamus and reticular
formation (and vice versa) and as a major link through which the hippocampus
and amygdala sometimes interact (Hagino & Yamaoka, 1976).
Amygdala interactions: The hippocampus is greatly influenced by the
amygdala, which in turn monitors and responds to hippocampal activity
(Gloor, 1955; Green & Adey, 1956; Steriade, 1964) (Figs. 23 - 25). The
amygdala also acts to relay certain forms of information from the
hippocampus to the hypothalamus (Poletti & Sajatanon, 1980). Together the
hippocampus and amygdala complement and interact in regard to attention, the
generation of emotional and other types of imagery, as well as learning and
memory.
Hippocampal Arousal, Attention, and Inhibitory Influences
Various investigators have assigned a major role to the hippocampus in
information processing, including memory, new learning, cognitive mapping of
the environment, voluntary movement toward a goal, as well as attention,
behavioral arousal, and orienting reactions (Douglas, 1967; Grastayan et
al., 1959; Green & Arduini, 1954; Isaacson, 1982; Milner, 1966, 1970, 1971;
Olton, Branch, & Best, 1978; Routtenberg, 1968). For example, hippocampal
cells alter their activity greatly in response to certain spatial
correlates, particularly as an animal moves about in its environment (Olton
et al., 1978). It develops slow-wave theta activity during arousal (Green &
Arduini, 1954) or when presented with noxious or novel stimuli (Adey,
Dunlop, & Hendrix, 1960). However, few studies have implicated this nucleus
as important in emotional functioning per se, although responses such as
"anxiety" or "bewilderment" have been observed when directly electrically
stimulated (Kaada, Jansen, & Andersen, 1954).
Hippocampal - Neocortical Interactions
Desynchronization of the cortical EEG is associated with high levels of
arousal and information input. As the level of input increases, the greater
the level of cortical arousal (Como, Joseph, Fiducia, & Siegel, 1979;
Joseph, Como, Forrest, Fiducia, & Siegel, 1981). However, when arousal
levels become too great, efficiency in information processing, memory, new
learning, and attention becomes compromised, as the brain becomes
overwhelmed.
When the neocortex becomes desynchronized (indicating cortical arousal),
the hippocampus often (but not always) develops slow-wave theta activity
(Grastayan et al., 1959; Green & Arduini, 1954) such that it appears to be
functioning at a much lower level of arousal. Conversely, when cortical
arousal is reduced to a low level (indicated by EEG synchrony), the
hippocampal EEG often becomes desynchronized.
These findings suggest when the neocortex is highly stimulated, the
hippocampus functions at a much lower level in order to monitor what is
being received and processed so as not to become overwhelmed. When the
neocortex is not highly aroused, the hippocampus presumably compensates by
increasing its own level of arousal so as to tune into information that is
being processed at a low level of intensity.
In situations in which both the cortex and the hippocampus become
desynchronized, distractability and hyperresponsiveness result and the
subject becomes overwhelmed and confused and may orient to and approach
several stimuli (Grastyan et al., 1959). Attention, learning, and memory
functioning are decreased. Such situations sometimes occur when one is
highly anxious, upset, or when traumatized. In fact, it is likely that the hippocampus might be injured by traumatic stress, which in turn would explain why some individuals become amnesic following a prolonged trauma (Joseph, unpublished 1980).
There is also evidence to suggest that the hippocampus may act to reduce
extremes in cortical arousal. For example, whereas stimulation of the
reticular activating system augments cortical arousal and EEG-evoked
potentials, hippocampal stimulation reduces or inhibits these potentials
such that cortical responsiveness and arousal are dampened (Feldman, 1962;
Redding, 1967). If cortical arousal is at a low level, hippocampal
stimulation often leads to augmentation of the cortical evoked potential
(Redding, 1967).
The hippocampal also exerts desynchronizing or synchronizing influences on
various thalamic nuclei, in turn augmenting or decreasing activity in this
region (Green & Adey, 1956; Guillary, 1955; Nauta, 1956, 1958). As the
thalamus is the major relay nucleus to the neocortex, the hippocampus
appears to be able to block or enhance information transfer to various
neocortical areas.
It is likely that the hippocampus may act to influence information
reception at the neocortical level as well as possibly reduce extremes in
cortical arousal (be they too low or high) via inhibition or excitation,
and/or it may act so that the neocortex is neither over- not underwhelmed
when engaged in the reception and processing of information. That is, very
high or very low states of excitation are incompatible with alertness and
selective attention and with the ability to learn and retain information
(Joseph et al., 1981).
Aversion and Punishment
In many ways, the hippocampus appears to act in concert with the medial
hypothalamus and septal nuclei (with which it maintains rich
interconnections) so as to prevent extremes in arousal and thus maintain a
state of quiet alertness (or quiescence). Moreover, as with the medial
hypothalamus, it has been reported that the subjective components of
aversive emotion in humans is correlated with electrophysiological
alternations in the hippocampus and septal area (Heath, 1976).
The hippocampus also appears to be heavily involved in the modulation of
reactions to frustrations or punishment (Gray, 1970), particularly in regard
to learning. For example, the hippocampus responds with trains of slow theta
waves when presented with noxious stimuli but habituates with repeated
presentation. Moreover, there is some evidence to suggest that this nucleus
in conjunction with the amygdala and septal nuclei is important in
generating negative cognitive-mood states such as anxiety.
Attention and Inhibition
The hippocampus participates in the elicitation of orienting reactions and
the maintenance of an aroused state of attention (Foreman & Stevens, 1987;
Grastayan et al., 1959; Green & Arduini, 1954; Routtenberg, 1968). When
exposed to novel stimuli or when engaged in active searching of the
environment, hippocampal theta appears (Adey et al., 1960). However, with
repeated presentations of a novel stimulus, the hippocampus habituates and
theta disappears (Adey et al., 1960). Thus, as information is attended to,
recognized, and presumably learned and/or stored in memory, hippocampal
participation diminishes. Theta also appears during the early stages of
learning as well as when engaged in selective attention and the making of
discriminant responses (Grastyan et al., 1959).
When the hippocampus is damaged or destroyed, animals have great difficulty
inhibiting behavioral responsiveness or shifting attention. For example,
Clark and Issacson (1965) found that animals with hippocampal lesions could
not learn to wait 20 sec between bar presses, if first trained to respond to
a continuous schedule. There is an inability to switch from a continuous to
a discontinuous pattern, such that a marked degree of perseveration and
inability to change sets or inhibit a pattern of behavior once initiated
occurs (Douglas, 1967; Ellen, Wilson, & Powell, 1964). Habituation is
largely abolished, and the ability to think or respond divergently is
disrupted.
In part, this finding suggests that hippocampal damage disrupts the ability
to learn and thus remember - findings that have been repeatedly demonstrated
in humans. In animals, disinhibition caused by hippocampal damage can even
prevent the learning of a passive-avoidance task, such as simple ceasing to
move (Kimura, 1958).
When coupled with the evidence presented above, it appears that the
hippocampus acts to enhance or diminish areas of neural excitation
selectively, which in turn allows for differential selective attention and
differential responding. When damaged, the ability to shift from one set of
perceptions to another or to change behavioral patterns is disrupted, and
the organism becomes overwhelmed by a particular mode of input. Learning,
memory, as well as attention are greatly compromised.
Learning and Memory
The hippocampus is most usually associated with learning and memory
encoding (e.g., long-term storage and retrieval of newly learned
information), particularly the anterior regions (Fedio & Van Buren, 1974;
Milner, 1966; 1970; Penfield & Milner, 1958; Rawlins, 1985; Scoville &
Milner, 1957). Many other brain areas, such as the mamillary bodies and
dorsal-medial nucleus of the thalamus, are also important in memory
functioning.
Bilateral destruction of the anterior hippocampus results in striking and
profound disturbances involving memory and new learning (i.e. , anterograde
amnesia). For example, one such patient who underwent bilateral destruction
of this nuclei (H.M.), was subsequently found to have almost completely lost
the ability to recall anything experienced after surgery. If you introduced
yourself to him, left the room, and then returned a few minutes later, he
would have no recall of having met or spoken to you. Dr. Brenda Milner has
worked with H.M. for almost 20 years, and yet she is an utter stranger to
him.
H.M. is in fact so amnesic for everything that has occurred since his
surgery (although memory for events prior to his surgery is comparatively
exceedingly well preserved), that every time he rediscovers that his
favorite uncle died (years after his surgery) he suffers the same grief as
if he has just been informed for the first time.
Despite his lack of memory for new (nonmotor) information, Henry (or H.M.),
has adequate intelligence, is painfully aware of his deficit, and constantly
apologizes for his problem. "Right now, I'm wondering" he once said, "Have I
done or said anything amiss?" You see, at this moment everything looks clear
to me, but what happened just before? That's what worries me. It's like
waking from a dream. I just don't remember.... Every day is alone in itself,
whatever enjoyment I've had, and whatever sorrow I've had.... I just don't
remember.
Presumably the hippocampus acts to protect memory and the encoding of new
information during the storage and consolidation phase via the gating of
afferent streams of information and the filtering/exclusion (or dampening)
of irrelevant and interfering stimuli. When the hippocampus is damaged,
input overload results, the neuroaxis is overwhelmed by neural noise, and
the consolidation phase of memory is disrupted such that relevant
information is not properly stored or even attended to. Consequently, the
ability to form associations (e.g., between stimulus and response) or to
alter preexisting schemas (such as occurs during learning) is attenuated
(Douglas, 1967).
Hippocampal and Amygdaloid Interactions: Memory
It has been argued that significant impairments involving memory (in man)
cannot be produced by lesions restricted to the hippocampus (cf. Horel,
1978). Thus, in some instances with restricted lesions, good recall of new
information is possible for at least several minutes (Horel, 1978; Penfield
& Milner, 1958). Rather, there is evidence that strongly suggests that the
hippocampus plays an interdependent role with the amygdala in regard to
memory (Kesner & Andrus, 1982; Mishkin, 1978; Sarter & Markowitsch, 1985).
Interestingly, nuclei such as the dorsal-medial region of the thalamus,
which have also been shown to be important in memory (Squire & Moore, 1979),
maintain rich interconnections with the amygdala (Krettek & Price, 1977b;
Nauta, 1971).
Nevertheless, although psychic blindness is produced by damage to the
amygdala, striking anterograde deficits in recall do not seem to occur
(Horel, 1978; Scoville & Milner, 1957). Rather, the role of the amygdala in
memory and learning seems to involve activities related to reward,
orientation, and attention, as well as emotional arousal (Sarter &
Markowitsch, 1985). If some event is associated with positive or negative
emotional states, it is more likely to be learned and remembered.
The amygdala seems to reinforce and maintain hippocampal activity through
the identification of motivationally significant information and the
generation of pleasurable rewards (through action on the lateral
hypothalamus). That is, reward increases the probability of attention being
paid to a particular stimulus or consequence as a function of its
association with reinforcement (Douglas, 1967; Kesner & Andrus, 1982).
However, the amygdala and hippocampus may act differentially in regard to
the effects of positive versus negative reinforcement on learning and
memory. For example, whereas the hippocampus produces theta in response to
noxious stimuli, the amygdale increases its activity following the reception
of a reward (Norton, 1970). Thus, if errors are made during acquisition
(negative emotional state), possibly the hippocampus modulates the
appropriate reaction, whereas when presented with a reward, the amygdala
reinforces the organism's response.
Thus, the hippocampus acts to reduce or enhance extremes in arousal
associated with information reception and storage in memory, whereas the
amygdala acts to identify the social-emotional-motivational characteristics
of the stimuli as well as to generate (in conjunction with the hippocampus)
appropriate emotional rewards to reinforce learning and memory. We find that
when both the amygdala and hippocampus are damaged, striking and profound
disturbances in memory functioning result (Kesner & Andrus, 1982; Mishkin,
1978).
Laterality
It is now very well known that lesions involving the mesial-inferior
temporal lobes (i.e., destruction or damage to the amygdala/hippocampus) of
the left cerebral hemisphere typically produce significant disturbances
involving verbal memory - particularly as contrasted with patients with
right-sided destruction. Left-sided damage disrupts the ability to recall
simple sentences and complex verbal narrative passages or to learn verbal
paired associates or a series of digits (B. Milner, 1966, 1970, 1971).
By contrast, right temporal destruction typically produces deficits
involving visual memory, such as the learning and recall of geometric
patterns, visual mazes, or human faces (Corkin, 1965; Milner, 1966; Kimura,
1963). Right-sided damage also disrupts the ability to recognize (through
recall) olfactory stimuli (Rausch, Serafetinides, & Crandall, 1977),
emotional sounds and passages (Wechsler, 1973), sounds from the environment,
as well as tactile mazes (Joseph, 1988a).
It appears, therefore, that the left amygdala/hippocampus is highly
involved in processing and/or attending to verbal information, whereas the
right amygdala/hippocampus is more involved in the learning, memory and
recollection of nonverbal, visual-spatial, environmental, emotional,
motivational, tactile, olfactory, and facial information.
THE PRIMARY PROCESS
Amygdaloid-Hippocampal Interactions during Infancy
Hallucinations
The amygdala-hippocampus complex, particularly that of the right
hemisphere, is very important in the production and recollection of
nonlinguistic images associated with past experience. In fact, direct
electrical stimulation of this region within the temporal lobes results not
only in the recollection of images but in the creation of fully formed
visual and auditory hallucinations (Halgren et al., 1978; Horowitz et al.,
1968; Malh et al., 1964; Penfield & Perot, 1963), as well as feelings of
familiarity (e.g., de ja vu).
Indeed, it has long been known that tumors invading specific regions of the
brain can trigger the formation of hallucinations that range from the simple
(flashing lights) to the complex. The most complex forms of hallucination,
however, are associated with tumors within the most anterior portion of the
temporal lobe (Critchley, 1939; Gibbs, 1951; Horowitz et al., 1968;
Tarachow, 1941), i.e., the region containing the amygdala and anterior
hippocampus.
Similarly, electrical stimulation of the anterior lateral temporal cortical
surface results in visual hallucinations of people, objects, faces, and
various sounds (Horowitz et al., 1968) - particularly the right temporal
lobe (Halgren et al., 1978). Depth electrode stimulation and thus direct
activation of the amygdala and/or hippocampus is especially effective.
For example, stimulation of the right amygdala produces visual
hallucinations, body sensations, de ja vu, illusions, as well as gustatory
and alimentary experiences (Weingarten et al., 1977). Conversely, Freeman
and Williams (1963) reported that the surgical removal of the right amygdala
in one patient abolished hallucinations. Stimulation of the right
hippocampus has also been associated with the production of deja-vu-,
memory-, and dreamlike hallucinations (Halgren et al., 1978), and in fact,
hallucinations seem to occur most frequently following hippocampal
activation (Horowitz et al., 1968).
As is well known, LSD can elicit profound hallucinations involving all
spheres of experience. Following the administration of LSD, high-amplitude
slow waves (theta) and bursts of paroxysmal spike discharges occur in the
hippocampus and amygdala (Chapman & Walter, 1965; Chapman, Walter, Ross et
al., 1963), but with little cortical abnormal activity. In both humans and
chimpanzees in whom the temporal lobes, amygdala, and hippocampus have been
removed, LSD ceases to produce hallucinatory phenomena (Baldwin et al.,
1959; Serafetinides, 1965). Moreover, LSD-induced hallucinations are
significantly reduced when the right versus left temporal lobe has been
surgically ablated (Serafetinides, 1965). Overall, it appears that the
amygdala, hippocampus, and the neocortex of the temporal lobe are highly
interactionally involved in the production of hallucinatory experiences.
Presumably, it is the neocortex of the temporal lobe that acts to interpret
this material (Penfield & Perot, 1963) as perceptual phenomena.
Dreaming
When hallucinations follow depth electrode or cortical stimulation, much of
the material experienced is very dreamlike (Halgren et al., 1978; Malh et
al., 1964) and consists of recent perceptions, ideas, feelings, and other
emotions that are similarly illusionary and dreamlike. Indeed, the right
hippocampus, and the right hemisphere in general (Broughton, 1982; Goldstein
et al., 1972; Hodoba, 1986; Humphrey & Zangwill, 1961; Kerr & Foulkes, 1978;
Meyer, Ishikawa, Hata, & Karacan, 1987), also appear to be involved in the
production of dream imagery as well as REM (at least in part) during sleep.
For example, there have been reports of patients with right cerebral
damage, hypoplasia, and abnormalities in the corpus callosum who have ceased
to dream altogether, suffer a loss of hypnotic imagery, or tend to dream
only in words (Botez, Olivier, Vezina, Botex, & Kaufman, 1985; Humphrey &
Zangwill, 1951; Kerr & Foulkes, 1981; Murri, Arena, Siciliano, Mazzotta, &
Muratorio, 1984). However, there have also been some reports that when the
left hemisphere has been damaged, particularly the posterior portions (i.e.,
aphasic patients), the ability to verbally report and recall dreams also is
greatly attenuated (e.g., Murri et al., 1984). Of course, aphasics have
difficulty describing much of anything, let alone their dreams.
Electrophysiologically, the right hemisphere also becomes highly active
during REM, whereas, conversely, the left brain becomes more active during
NREM (Goldstein et al., 1972; Hodoba, 1986). Similarly, measurements of
cerebral blood flow have shown an increase in the right temporal regions
during REM sleep in subjects who upon wakening report visual, hypnagogic,
hallucinatory, and auditory dreaming (J.S. Meyer et al., 1987).
Interestingly, abnormal and enhanced activity in the right temporal and
temporal - occipital area acts to increase dreaming and REM sleep for an
atypically long time period (Hodoba, 1986). Thus, it appears that there is a
specific complementary relationship between REM sleep and right temporal
electrophysiological activity.
In addition, during REM, the hippocampus begins to produce slow wave, theta
activity (Jouvet, 1967; Olmstead, Best, & Mays, 1973; Robinson, Kramis, &
Vanderwolf, 1977). Presumably, during REM, the hippocampus acts as a
reservoir from which various images, words, and ideas are drawn and
incorporated into the matrix of dreamlike activity being woven by the right
hemisphere. It is probably just as likely that the hippocampus serves as a
source from which material is drawn during the course of a daydream.
Interestingly, daydreams appear to follow the same 90- to 120-min cycle
that characterize the fluctuation between REM and NREM periods, as well as
fluctuations in mental capabilities associated with the right and left
hemisphere (Broughton, 1982; Kripke & Sonneschein, 1973). That is, the
cerebral hemispheres tend to oscillate in activity every 90- 120 min - a
cycle that appears to correspond to the REM - NREM cycle and the appearance
of day and night dreams.
Dreams and Infancy
In the newborn, and up until approximately 6 - 9 months, there are two
distinct stages of sleep which correspond to REM and N-REM periods
demonstrated by adults (Berg & berg, 1978; Dreyfus-Brisac & Monod, 1975;
Parmlee, Wenner, Akimaya, Schults, & Stern, 1967). Among infants, however,
REM occur during wakefulness as well as during sleep. In fact, REM can be
observed when the eyes are open, when the infant is crying, fussing, eating,
or sucking (Emde & Metcalf, 1970). Moreover, REM is also observed to occur
within a few moments after an infant begins to engage in nutritional sucking
and appears identical to that which occurs during sleep (Emde & Metcalf,
1970).
The production of REM during waking in some respects seems paradoxical and
a number of different mechanism are no doubt responsible. Nevertheless, it
might be safe to assume that like an adult, when the infant is in REM, he or
she is dreaming, or at least, in a dreamlike state. This state might
correspond to what Freud described as the primary process. That is, when
produced when the infant is crying or fussing, it is dreaming of whatever
relief it seeks. Correspondingly, REM that occurs while eating or sucking
may have to do with the limbic structures involved not only in the
production of dreamlike activity, but the identification, learning, and
retention of motivationally significant information (i.e., the amygdala and
hippocampus).
The Primary Process
The hypothalamus, our exceedingly ancient and primitive Id, has an "eye"
that only sees inward. It can tell if the body needs nourishment but cannot
determine what might be good to eat. It can feel thirst, but has no way of
slaking this desire. The hypothalamus can only say: "I want," "I need," and
can only signal pleasure and displeasure. However, as the seat of pleasure,
the hypothalamus can be exceedingly gracious in rewarding the organism when
its needs are met. Conversely, when its needs go unmet, it can respond not
only with displeasure and feelings of aversion, but with undirected fury and
rage. It can cause the organism to cry out. However, the cry does not
produce the immediately desired relief or reduction in tension. Pressure is
exerted on the limbic system and the organism to engage in environmental
surveillance so as to meet the needs monitored by the hypothalamus.
Over the course of the first months of life, as the amygdala and then the
hippocampus develop, the organism begins to develop an eye that not only
sees outward but that can register and recall events, objects, people, and
so forth associated with tension reduction, pleasure, and the satiety of the
infants internal needs (e.g., the taste, smell, feeling of mother's breast
and milk, the experience of sucking and relief). This is called learning.
With the maturation of these two limbic nuclei, the infant is increasingly
able to differentiate what occurs in the external environment based on
hypothalamically monitored needs and the emotional/motivational significance
of that which is experienced. The infant can now orient, selectively attend,
determine what brings satisfaction, and store this information in memory.
Primary Imagery
Although admittedly we have no direct knowledge as to the psychic
interactions in the neonate, it does seem reasonable to assume that as the
neocortex and underlying structures and fiber pathways mature, neural
"programs" are formed that correspond to the repeated registration of
experiences which are deemed significant (e.g., pleasurable). That is,
neural pathways that are repetitively fired, deactivated, or activated in
response to specific sensory and affective activities and experiences,
become associated with that activity, such that an associated neural circuit
is formed (Joseph, 1982; Penfield, 1954; Spinelli, 1970); i.e., a memory is
created. Eventually, if this circuit is reactivated, the "learned" pattern
is reexperienced; i.e., the organism remembers.
Thus, when the amygdala/hippocampus is stimulated by a hungry hypothalamus,
the events and images associated with past experiences of pleasure not only
can be searched out externally but can be recalled in imaginal form. For
example, as an infant experiences hunger and stomach contractions as well as
its own cries of displeasure, these states become associated with the sound,
smell, taste, and other cues of mother and her associated movement, as well
as other stimuli that accompany being fed (cf. Piaget, 1952, pp. 37,
407-408). Repetitively experienced, the sequence from hunger to satiety
evokes and becomes associated with the activation of certain neural
pathways.
Eventually, when the infant becomes hungry and that hunger is prolonged,
the entire neural sequence associated with hunger and feeding (i.e., hunger,
mother, food, satiety) may become involuntarily triggered and activated
(through association) such that an "image" of being fed is experienced. The
activation of these rudimentary and infantile memory images is probably what
constitutes, at least in part, the primary process.
Behaviorally, this is manifested by REM and by sucking and tongue movements
as if eating, when in fact no food is present (cf. Piaget, 1952). When
hungry, the infant will begin to cry and REM might be observed; the infant
will then stop crying and smack its lips and make sucking movements
(mediated by the amygdala) as if it were being fed. The infant experiences
being fed in the form of a dream (Joseph, 1982) or hallucination.
The brain of the human infant is quite immature for several years, in turn
restricting information reception and processing (Joseph, 1982; Joseph,
Gallagher, Holloway, & Kahn, 1984); also, given the limited amount of
reality contact infants are able to achieve, these rudimentary memories and
images (even when they occur during waking, i.e., REM) are probably
indistinguishable from actual experience simply because they are experience.
Like a dream, when replayed, the infant presumably reexperiences to some
degree the sensations, emotions, and so forth originally linked to tension
reduction. Thus, the young infant, still unable to distinguish between
representation and reality, responds to the image as reality (Freud, 1911),
even while awake - as manifested by REM. When hunger is prolonged, the
associations linked to feeding are triggered, and for a brief period the
infant behaves as if its hunger has been sated. Reality is replaced by an
image, or rather, a "dream." This is the primary process.
Since the hypothalamus (which monitors internal homeostasis) is not
conscious that the dream images experienced are not real, it initially
accepts the memory/dream images transmitted from the amygdala and
hippocampus and ceases to cry, i.e., it responds to the imagined sources of
nourishment just as it responds to a cue tone associated with a food reward
(Nakamura & Ono, 1986; Ono et al., 1980). However, the hypothalamus is not
long fooled, for the primary process does not offer effective long-lasting
relief from tension. As the pain of hunger remains and increases, limbic
activity is increased, and the image falls away, to be replaced by a cry of
hunger (Joseph, 1982). The amygdala and hippocampus are thus forced to renew
their surveillance of the environment in search of sources of tension
reduction. Cognitive development is thus promoted (Freud, 1911):
Whatever was thought of (desired) was simply imagined in an hallucinatory
form, as still happens today with our dream-thoughts every night. This
attempt at satisfaction by means of hallucination was abandoned only in
consequence of the absence of the expected gratification, because of the
disappointment experienced. Instead, the mental apparatus had to decide to
form a conception of the real circumstances in the outer world and to exert
itself to alter them.... The increased significance of external reality
heightened the significance also of the sense-organs directed towards the
outer word, and of the consciousness attached to them; the later now learned
to comprehend the qualities of sense in addition to the qualities of
pleasure and "pain" which hitherto had alone been of interest to it. A
special function was instituted which had periodically to search the outer
word in order that its data might be already familiar if an urgent need
should arise; this function was attention. Its activity meets the
sense-impressions halfway, instead of awaiting their appearance. At the same
time there was probably introduced a system of notation, whose task was to
deposit the results of this periodical activity of consciousness - a part of
that which we call memory. (pp. 410-411)
SEPTAL NUCLEI
Phylogenetically, the septal nuclei develops following the appearance of
the amygdala, at about the same time and rate as the hippocampus (Andy &
Stephan, 1976; Brown, 1983; Humphrey, 1972). It also increases in relative
size and complexity as we ascend the ancestral tree, attaining its greatest
degree of development in humans.
Specifically, the septal nuclei lie in the medial portions of the
hemispheres, just anterior to the third ventricle near the hypothalamus. The
septum projects heavily throughout the hypothalamus and maintains rich
interconnections with all regions of the hippocampus (Mesulam, Mufson,
Levey, & Wainer, 1983; Siegel & Edinger, 1976). It also contributes to and
receives fibers from the amygdala via the stria terminalis (Swanson & Cowan,
1979) and receives and gives rise to one of the most massive roots of the
medial forebrain bundle through which it receives olfactory and ascending
brainstem (reticular formation) fibers (Nauta, 1956).
Aversion and Internal Inhibition
In general, the septal nucleus appears to act in conjunction with the
medial hypothalamus and hippocampus, particularly as related to internal
inhibition and the exertion of quieting and dampening influences on arousal
and limbic system functioning. In this regard, the septum appears to
counterbalance some aspects of amygdaloid and lateral hypothalamic activity
while simultaneously facilitating the actions of the hippocampus and media
hypothalamus (Kolb & Whishaw, 1977; Mogenson, 1976; Petsche, Gogolack, & Van
Zwieten, 1965; Petsche, Stumpf, & Gogolack, 1962).
Specifically, depending on the level of hypothalamic arousal, the septum
exerts facilitatory or inhibitory influences on this nuclei (Mogenson, 1976)
and from impulses it receives and relays from the reticular activating
system, mediates and greatly influences hippocampal activity as well (Kolb &
Whishaw, 1977; Petsche et al., 1962, 1965). The septal region (along with
that of the hippocampus and medial hypothalamus) has also been reported in
humans to show electrophysiological alterations in activity that correspond
to subjective feelings of aversion (Heath, 1976).
The septum and amygdala appear to enjoy largely an antagonistic
relationship, particularly in regard to influencing the hypothalamus. For
example, the amygdala acts either to facilitate or to inhibit septal
functioning, whereas septal influences on the amygdala are largely
inhibitory. However, in large part, the amygdala and septal nuclei appear to
exert most of their counterbalancing influences at the level of the
hypothalamus, particularly in regard to emotionality.
Quiescence
A primary activity of the septal nucleus appears to be that of reducing
extremes in emotionality and arousal and maintaining the organism in state
of quiescence and readiness to respond. Stimulation of the septum acts to
reduce blood pressure and heart rate and to induce adrenocortical secretion
(Endroczi, Schreiberg, & Lissak, 1963; Kaada, 1951; Ranson, Kabat, & Magoun,
1935). It also counters lateral hypothalamic self-stimulatory activity
(Mogenson, 1976).
Rage
Electrical stimulation of the septum counters and inhibits aggressive
behavior (Rubenstein & Delgado, 1963) and suppresses the expression of rage
reactions following hypothalamic stimulation (Siegel & Edinger, 1976).
If the septal nucleus is destroyed, these counterbalancing influences are
removed such that initially dramatic increases in aggressive behavior,
including rage (Ahmad & Harvey, 1968; Blanchard & Blanchard, 1968; Brady &
Nauta, 1953; King, 1958), results. Bilateral lesions in fact give rise to
explosive emotional reactivity to tactile, visual, or auditory stimulation,
which can take the form of attack (fight) or flight. If the amygdala is
subsequently lesioned, the septal rage and emotional reactivity are
completely attenuated (King & Meyer, 1958). Thus, septal lesions appear to
result in a loss of modulatory and inhibitory restraint.
Septal Social Functioning
Eventually, within a few weeks or months, rage and aggressiveness due to
septal lesions subside and/or completely disappear. However, a generalized
tendency to overrespond and a generalized failure to inhibit emotional
responsiveness persist (McClary, 1961; 1966; Poplawsky, 1987). In
particular, rather than rage or irritability, septal lesions produce
indiscriminant socializing and an extreme need for social and physical
contact (Jonason & Enloe, 1971; Jonason et al., 1973; McClary, 1961, 1966;
Meyer, Ruth, & Lavond, 1978).
Socialization and Contact Comfort
In contrast with amygdaloid lesions, which produce a severe
social-emotional agnosia and social avoidance, septal lesions produce a
dramatic and persistent increase in social cohesiveness (Jonason & Enloe,
1971; Jonason et al., 1973; D. R. Meyer et al., 1978). Thus, the normal
intact amygdala appears to promote social behavior, whereas the septal
nucleus seems to counter socializing tendencies.
With complete bilateral destruction of the septum in animals, the drive for
social contact appears to be irresistible such that persistent attempts to
make physical contact occur - even with species quite unlike their own. This
occurs because the amygdala (as well as other nuclei) are no longer opposed
by the septal nucleus.
Ritchie (1975, cited by D. R. Meyer et al., 1978)reported that septally
lesioned rats, unlike normals, will readily seek out mice (to which they are
normally indifferent) or rabbits (which they usually avoid). If presented
with a choice of an empty (i.e., safe) chamber or one containing a cat,
septally lesioned rats persistently attempt to huddle and crawl upon this
normally feared creature, even when the cat is acting perturbed. If a group
of septally lesioned animals are placed together, extreme huddling results.
So intense is this need for contact comfort following septal lesions that if
other animals are not available they will seek out blocks of wood, old rags,
bare wire frames, or walls.
Among humans with right-sided or bilateral disturbances in septal
functioning (such as due to seizure activity generated in this region), a
behavior referred to as stickiness is sometimes observed. Such individuals
seek to make repeated, prolonged, and often inappropriate contact with
anyone who is available or who happens to be nearby so as to tell them
stories or jokes or merely pass the time. They seem to have little actual
concern regarding the feelings of others or how interested they might be in
interacting. Indeed, they do not readily take a hint and are difficult to
get rid of. In hospital situations, they can be found intruding on other
patients and their families, hanging out by the nurse's station, or
incessantly visiting other rooms to chat.
Attachment and Amygdaloid - Septal Developmental Interactions
Broadly considered, the various nuclei comprising the limbic system
demonstrate functional maturity at different rates. Correspondingly, certain
behaviors and capacities appear at various time periods, overlay previous
capacities, become differentiated, and/or in turn become suppressed or
eliminated.
At birth the hypothalamus reins supreme in regard to emotion. The infant
freely expresses feelings of aversion and rage or pleasure or quiescence and
demonstrates extreme orality and other behaviors similar to a state in which
the amygdala is functionally nonexistent.
As the amygdala and hippocampus begin to develop and mature, the organism
becomes more reality oriented and more social as the ability to attend
selectively to externally occurring events and to store this information in
memory becomes more pronounced. The pleasure principle (although still
dominant) begins to be served by the reality principle (Freud, 1911).
Since the development of the amygdala precedes that of the septal nuclei,
social-emotional activities mediated by the amygdala are expressed in an
uninhibited fashion. That is, when the counterbalancing influences of the
septum are absent (as a result of surgical removal or functional
immaturity), the behavior expressed is in many respects similar to that
expressed by infants, for example, indiscriminant contact seeking (e.g.,
attachment behavior).
Attachment
Attachment is not the same as dependency. Necessarily, the infant is
dependent on its caretaker (e.g., mother). However, until the child is 6-7
months of age, it will smile at the approach of anyone, even complete
strangers, and will vigorously protest any form of separation from these
unknown people (e.g., if they leave the room). This state corresponds to
the amygdaloid development period, during which septal influences are
largely nil.
At about 7 months of age, the infant becomes more discriminant in its
interactions and it is during this time period that a very real and specific
attachment is formed, e.g., to one's mother - an attachment that becomes
progressively more intense and stable. This period represents initial septal
developmental influences such that global contact seeking becomes
increasingly narrowed and restricted.
After these specific attachments have been formed, children begin to show
anxiety, fear, and even flight reactions at the approach of a stranger
(Spitz & Wolf, 1946). By 9 months, 70% of children respond aversively,
whereas by 10 months they might cry out if a stranger were to appear
(Schaffer, 1966; Waters, Matas, & Sroufe, 1975). By 1 year of age, 90% of
children respond aversively to strangers (Schaffer, 1966).
Thus, during the amygdaloid phase there is indiscriminant approach and
contact seeking. During the septal stage, indiscriminant social contact
seeking is inhibited, whereas the specific attachments already formed are
strengthened, reinforced, and maintained. The differential rates of amygdala
and septal development are thus crucial in promoting survival and social
interaction with significant others.
Their differential maturation rates also represent critical time periods,
which in turn require specific interactional social-physical forms of
stimulation, such as the presence and care of a primary caretaker. If these
interactional needs are not met during the critical development period,
gross abnormalities can result.
Indeed, if contact with others is restricted during these early phases, the
ability to socially interact successfully at a later stage of development is
retarded. This is even true among the so-called lower animals. For example,
kittens that are not exposed to humans grow up to be wild and
unapproachable. The phenomena of imprinting probably also requires that
similar interactions take place.
Contact Comfort
As is well known, for the first 6-8 months of life, physical and social
interaction with others is critical in regard to psychological,
neurological, and physical development. During this period (which
corresponds to the amygdaloid phase of maturation), contact seeking is
indiscriminant. However, indiscriminant contact seeking and attachment
during early development maximizes opportunities for physical - social
interaction. So intense is the need for physical and social contact that
young animals will form attachments to bare wire frames (Harlow, 1962), to
television sets, to dogs that might maul them, and to creatures that might
kill them (Cairn, 1966). Young human children will form attachments to
mothers who might abuse them. With removal of the septum, animals will even
seek contact with creatures that might eat them.
So pervasive is this need for physical interaction (especially among
humans) that, when grossly reduced or denied, the result is often death. For
example, in several well-known studies of children raised in foundling homes
during the early 1900s, when the need for contact was not well recognized,
morbidity rates for children under 1 year of age were more than 70%. Of
10,272 children admitted to the Dublin Foundling home during a single
25-year period, only 45 survived (Langmeier & Matejcek, 1975, for review).
Of those who have survived an infancy spent in institutions in which
mothering and contact comfort were minimized, signs of low intelligence,
extreme passivity, apathy, as well as severe attentional deficits are often
characteristic (Dennis, 1960; Langmeier & Matejcek, 1975; Spitz, 1945). Such
individuals have difficulty forming attachment or maintaining social
interactions later in life.
In his famous series of experiments with monkeys, Harlow (1962) also showed
that even those raised with surrogate terry cloth mothers develop extremely
bizarre behaviors:
The laboratory monkeys sit in their cages and stare fixedly into space,
circle their cages in a repetitive stereotyped manner and clasp their heads
in their hands or arms and rock for long periods of time. They often develop
compulsive habits, such as pinching precisely the same patch of skin on
their chest between the same fingers hundreds of times a day; occasionally
such behavior may become punitive and the animal may chew and tear at its
body until it bleeds.
It is noteworthy that the maternal behavior of chimpanzees raised in
isolation is also quite abnormal and in fact similar to that of mothers who
have had their amygdalas destroyed. As described by Harlow (1965):
After the birth of her baby, the first of these unmothered mothers ignored
the infant and sat relatively motionless at one side of the cage, staring
fixedly into space hour after hour. As the infant matured desperate attempts
to effect maternal contact were consistently repulsed.... Other motherless
monkeys were indifferent to their babies or brutalized them, biting off
their fingers or toes, pounding them, and nearly killing them until
caretakers intervened. One of the most interesting findings was that despite
the consistent punishment, the babies persisted in their attempts to make
maternal contact.
Deprivation and Amygdaloid - Septal Functioning
In addition to mediating all aspects of higher-order emotional functioning,
the amygdala is particularly responsive to tactual stimulation such that
single cells may respond to touch, regardless of where on the body the
person was stimulated. When there is inadequate tactile and physical-social
interaction during early development, the ability of these cells to develop
and function adequately is significantly reduced. That is, the amygdala (as
well as other nuclei) becomes environmentally damaged.
As has been repeatedly demonstrated in studies of the visual system as well
as on cerebral development, one consequence of reduced environmental input
during certain critical periods of development is cell death, atrophy, and
functional retardation, as well as inhibition by competing neuronal cell
assemblies (Casagrande & Joseph, 1980; Greenough, 1976; Rosenzweig, 1971).
Consequently, gross behavioral and perceptual abnormalities result (Harlow,
1962; Joseph & Casagrande, 1980; Joseph & Callagher, 1982).
For example, if the lids of one eye are surgically sutured shut, patterned
visual input is prevented from reaching target cells in the lateral
geniculate nucleus of the thalamus. When this occurs target neurons become
smaller, fewer in number, and functionally suppressed by adjacent cells
receiving normal input. If the sutures are reversed such that the formerly
deprived eye is opened, the subject responds as if blind. However, if the
normal eye is surgically removed, some vision returns to the formerly
deprived eye, and some functional neuronal recovery is observed (Casagrande
& Joseph, 1980), presumably because of the removal of inhibitory influences.
This deprivation effect is only noted to occur during the first few months
after birth in primates.
Given the similarity in social unresponsiveness and disturbances in
maternal behavior demonstrated by amygdalectomized and socially-maternally
deprived primates, it is likely that like the visual system, abnormalities
in cellular development and function also occur within the amygdala and
septum secondary to deprivation. Unfortunately, few researchers have
explored this line of inquiry.
Nevertheless, it has been demonstrated that the right amygdala is larger
than the left in animals reared in enriched and normal environments, whereas
these differences are nonsignificant in animals reared in a restricted
setting (Diamond, 1985), suggesting that deprivation differentially reduces
right amygdaloid growth. This finding is significant because among humans,
the right cerebral hemisphere has been shown to be dominant in regard to
most aspects of social-emotional functioning. (See Chapter 1, The Right
Cerebral Hemisphere.)
Heath (1972) also noted that the monkeys reared without mothers develop
abnormal spiking in the septal region. Similarly, Heath (1954) found
abnormal seizurelike discharges in the septum of withdrawn schizophrenics,
noting that the severity of the abnormality was correlated with the severity
of the psychosis.
Among those with normal limbic systems, it is presumably the interaction of
these same nuclei that gives rise to attachment and bonding behavior in
adults. Moreover, it is probably through the interactions mediated by these
nuclei that emotions such as jealousy are generated. That some individuals
respond with considerable grief, anger, and even uncontrollable rage when a
"loved one" has ended a relationship probably can also be explained from a
limbic perspective.
THE UNCONSCIOUS MIND
The limbic system, as defined in this paper, provides the foundations for
the development of not only emotion, but social-psychological functioning as
well as the more rudimentary aspects of unconscious mental activity. The
limbic system, however, represents the most primitive features of the
unconscious. A second, more highly developed, unconscious (i.e.,
nonlinguistic) mind is maintained via the functional interactions of the
right cerebral hemisphere (Joseph, 1988a, b); however this mental realm only
seems to be unconscious from the perspective of the left cerebral
hemisphere. Nevertheless, because the interaction of various limbic nuclei
is also important in learning and memory, as well as social-emotional
functioning, it is likely that a variety of neurotic disturbances, needs,
desires, and insecurities have as their foundation events differentially
experienced and attended to by the limbic system.
This seems particularly true regarding events experienced during infancy
and early development. For example, it is well known that most events
experienced before age 4 are extremely difficult to recall. In part this is
because of the different modes of information processing and coding employed
by adults versus children (Joseph, 1988a). That is, much of what was
experienced, learned, and stored in memory during early childhood occurred
before the development of language. Thus, adults, relying on language, can
no longer access the code in which this early information was stored. The
key no longer fits the lock.
Nevertheless, because the limbic system of both an adult and infant uses
nonlinguistic social-tactual-emotional-visual forms of information
processing and expression, much of what occurs at this level falls outside
the immediate jurisdiction of the conscious mind, which relies predominantly
on language and rational, temporal-sequential linguistic thought for
understanding.
Because of this, we may feel angry or sad and not consciously (i.e.,
linguistically) know why. However, at a limbic level, we may feel anxious or
angry because something was seen, heard, or even smelled, which called forth
old limbic memories of some unpleasant event - memories that are not
accessible to the linguistic mind.
Take, for example, a young child, who, like many infants, at times
manipulated her genitalia. Unfortunately, this little girl's mother (being
very repressed and rigid) responded with shock and disgust when she
discovered her daughter's action. Resolving to put an end to this "repulsive
behavior," the mother shouted "No" in an angry voice and slapped the child
every time her daughter touched herself.
Soon the behavior was abolished through simple stimulus - response
learning. This is because, at a limbic level, every time the urge to touch
the genitalia arose, the behavior was severely punished. The child's urge to
touch became associated with physical pain, and later with the anxiety of
anticipated pain. Only three nuclei are necessary to form this circuit - the
hypothalamus, amygdala, and hippocampus - as it is purely emotional and
without thought. Indeed, much of this learning can probably occur without
amygdaloid or hippocampal involvement, in which case the memory may remain unconscious. In fact, if sufficiently traumatized, the hippocampus (as well as the amygala) might be damaged (Joseph, unpublished observations), thus resulting in unconscious learning and memories that remain unconscious and which cannot be recalled due to trauma and hippocampal induced amnesia.
Nevertheless, as an adult, this young woman now has difficulty associating
with men, as sometimes their mere presence brings forth terrible feelings of
anxiety. She has one failed relationship after another, and soon discovers
herself to be frigid. She hates sex, she hates to be touched, and men repell
her.
Consciously, she may be able to generate a panoply of explanations, all of
which, at some level, are believable, albeit erroneous. Consciously, she has
no true idea as to the source of her difficulties. Nevertheless, at the
limbic level, the explanation is very basic. Certain men trigger the onset
of amorous feelings. Unfortunately, the woman never feels sexually aroused.
The first inklings of arousal immediately generate feelings of anxiety and
limbic memories of physical pain. This is what she experiences and responds
to.
CONCLUSION
A variety of nuclei and brain regions are important in emotional
functioning. In this chapter, only a few of these regions are discussed. In
some respects, many might argue that such structures as the hippocampus
should not be considered part of the limbic system because of its
involvement with memory. Indeed, it has become increasingly fashionable to
decry even the use of the term limbic system, as there are simply so many
diverse cerebral regions involved in the control and mediation of emotional
functioning. Even by the most liberal of anatomical definitions there can be
no structural basis for the concept when all such nuclei are considered.
This is not the case, however, in regard to the highly interactional
anatomical and functional system maintained by the amygdala, hypothalamus,
hippocampus, and septal nuclei. Therefore, I encourage continued use of the
term, particularly in that to most people limbic system implies that part of
the "old" brain concerned with emotional functioning.
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