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From: Neuropsychiatry, Neuropsychology, Clinical Neuroscience (Academic Press, New York, 2000)
by Rhawn Joseph, Ph.D.


Memory & Attention

The hippocampus (Ammon's Horn" or the "sea horse") is an elongated structure located within the inferior medial wall of the temporal lobe (posterior to the amygdala) and surrounds, in part, the lateral ventricle. In humans it consists of an anterior and posterior region and depending on the angle at which it is viewed, could be construed as shaped somewhat like an old fashion telephone receiver, or a "sea horse." The hippocampus consists of a number of subcomponents, and adjoining structures, such as the parahippocampal gyrus, entorhinal and perirhinal cortex and the uncus (which it shares with the amygdala) are considered by some to be subdivisions, whereas the main body of the hippocampus consists of the dentate gyrus, the subiculum, and sectors referred to as CA1, CA2, CA3, CA4.

The uncus is a bulbar allocortical protrusion located in the anterior-inferior medial part of the temporal lobe, and consists of both the hippocampus and amygdala which become fused in forming this structure. That is the ventral-medial portion of the amygdala becomes fused with the head of the hippocampus, such that the uncus consists of both allocortex and mesocortex--the entorhinal cortex which shrouds the hippocampus.

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 cingulate, and via the entorhinal area--the mesocortical gateway to the hippocampus. It is through the fornix-fimbrial pathways that the hippocampus makes major interconnections with the thalamus, septal nuclei, medial hypothalamus, and via which it exerts either inhibitory or excitatory influences on these nuclei (Feldman et al. 1987; Guillary, 1957; Poletti & Sujatanon, 1980; Risvold & Swanson, 1996).

Essentially, the fornix and fimbria are one and the same, as the fornix becomes the fimbria as they arch together near the tail of the hippocampus, with the fornix continuing its journey jutting beneath the corpus callosum where it meets the contralateral fornix from the contralateral tail of the hippocampus. It is at this junction that the fornix distributes massive axonal fibers to the medially located septal nuclei (the septum pellucidum).

Thus, the hippocampus maintains a particularly intimate relationship with the septal nuclei via the fornix, such that the tail of the hippocampus is directly connected with the septal nuclei which then relays hippocampal impulses to the hypothalamus (and back again); which in turn may enable these structures to form conjunctions between those external events which are memorable with internal homeostatic events which preceded, coincided, or followed. 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 (Gloor, 1997; Hagino & Yamaoka, 1976).

The entorhinal cortex acts to relays information to and from the hippocampus. It is through the entorhinal cortex that the hippocampus maintains interconnections with the neocortical multi-modal associations areas of the temporal, frontal, and parietal lobes, including surrounding structures, e.g., the parahippocampal gyrus, and allocortical tissues, the perirhinal cortex, septal nuclei and amygdala (Amaral et al. 1992; Carlsen et al. 1982; Gloor, 1955; Krettek & Price, 1976; Murray 1992; Steward, 1977; Van Hoesen et al. 1972). The parahippocampal gyrus, entorhinal and perirhinal cortex, being directly interconnected with the hippocampus and the neocortex, act to relay input from the neocortical association areas to this structure. In fact, they interact so intimately with the hippocampus that some investigators considered them as part of the "hippocampal system." The "hippocampal system" however, is considerd by some to also include the amygdala, dorsal medial nucleus, the septal nuclei, and the hypothalamus and brainstem. Hence, when considered broadly, the "hippocampal" system could be viewed as forming a unified substrate that subserves the non-motor aspects and declarative aspects of memory (Gloor, 1997).

The entorhinal cortex, particular, is a major component of the "hippocampal system." This structure is truly unique, not only because it serves as an interface between the hippocampus and the neocortex, but because this medial located structures consists of between 7 and 8 layers (Braak & Braak, 1992; Ramon y Cajal, 1902/1955; Rose, 1926). The entorhinal cortex also maintains massive interconnections with all multi-modal neocortical association areas (as well as with the amygdala, hippocampus, septal nuclei, olfactory bulb, etc.) but apparently none of the primary sensory areas (Leichnetz & Astruc, 1976; van Hoesen, et al., 1975). Hence, the entorhinal cortex must play a supramodal role that is exceedingly unique and profoundly important in memory and cognitive processing. However, as to its exact role is difficult to determine, as it is difficult, if not impossible to cut away the entorhinal cortex from the hippocampus without damaging or deinnervating both. Nevertheless, presumably they subserve different aspects of memory.

As noted, the amygdala, septal nuclei, as well as the parahippocampal gyrus also maintains direct interconnections with the hippocampus as well as with each other and often overlapping neocortical areas, such as the orbital frontal lobe. The hippocampus is greatly influenced by the amygdala which in turn monitors and respondes to hippocampal activity (Gloor, 1955, 1992, 1997; Green & Adey, 1956; Halgren 1992; Steriade, 1964). Indeed, the amygdala may act to alert the hippocampus to stimuli or events which are emotionally significant so that the hippocampus "pays attention" and stores the non-emotional attributes in memory. The amygdala also acts to relay certain forms of information from the hippocampus to the hypothalamus (Poletti & Sajatanon, 1980), thus forming an emotional-cognitive circuit which may enable the organism to relate external events to internal events, and to then store this integrated information in memory; for example a particular tasty food items (or prey) that was discovered in a certain spatial location. The hippocampus and amygdala thus interact in regard to attention, the generation of emotional and other types of imagery, as well as learning and memory.

Since the amygdala becomes fused with the head of the hippocampus, and as they also interact via the entorhinal cortex, it is difficult, if not impossible to cut away one structure from the other without damaging or deinnervating both. Hence, those studies which claim to remove the amygdala while sparing the hippocampus, or vice versa, and/or to have removed these structures while sparing the entorhinal cortex, and the claims made by these investigators regarding the results of these studies, must be viewed with a measure of skepticism (see Gloor, 1997, for related discussion).

Nevertheless, it was reported by Scoville and Milner (1957), in their classic paper which revolutionized thinking as to the role of the hippocampus in memory, that although the surgical destruction of the hippocampus and amygdala (plus the uncus and parahippocampal gyrus) resulted in profound amnesic syndrome, that similar deficits were not observed when just the uncus, the amygdala, and head of the hippocampus were removed. On the other hand, these tissues were removed because they were abnormal, and as the amygdala is often the source of temporal lobe seizures (Gloor, 1997), including even seizure-induced damage to the hippocampus, the findings of Scoville and Milner (1957) and Penfield and Milner (1958), and all related papers regarding the removal of damage tissue, must be viewed with caution as they may not be generalizable to the normal amygdala and hippocampus. Due to neuroplasticity other structures may have taken over the "normal" functions of the amygdala, such that in consequence, there is no memory loss as those aspects of memory associated with the the amygdala are now subserved by another region of the brain. Indeed, there is no general consensus as to the role of the hippocampus (or the amygdala) in memory, and the interested reader is directed to the special issues of the journal, Hippocampus (Vol. 1, #3) and the Journal of Cognitive Neuroscience (Vol. 4, # 3), where various protagonists lay out their differing views.


Various authors have assigned the hippocampus a major role 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; Eichenbaum et al. 1994; Enbert & Bonhoeffer, 1999; Frisk & Milner, 1990; Grastayan et al., 1959; Green & Arduini, 1954; Isaacson, 1982; Milner, 1966, 1970, 1971; Nishitani, et al., 1999; Olton et al. 1978; Routtenberg, 1968; Squire, 1992; Victor & Agamanolis, 1990; Xu et al., 1998). For example, hippocampal cells greatly alter their activity in response to certain spatial correlates, particularly as an animal moves about in its environment (Nadel, 1991; O'Keefe, 1976; Olton et al., 1978; Wilson & McNaughton, 1993). It also developes slow wave theta activity during arousal (Green & Arduini, 1954) or when presented with noxious or novel stimuli (Adey et al.1960)--at least in non-humans.

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 et al. 1953). Indeed, in response to persistent and repeated instances of stress and unpleasant emotional arousal, the hippocampus appears to cease to participate in cognitive, emotional, or memory processing (chapter 30). Thus the role of the hippocampus in emotion is quite minimal.


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 is the level of cortical arousal (Como et al. 1979; Joseph et al. 1981; Joseph, 1998b, 1999d). However, when arousal levels become too great, efficienty in information processing, memory, new learning, and attention become compromised as the brain becomes overwhelmed (Joseph, 1998b, 1999d; Joseph et al., 1981; Lupien & McEwen, 1997; Sapolsky, 1996).

When the neocortex becomes desynchronised (indicating cortical arousal), the hippocampus often (but not always) developes slow wave theta activity (Grastyan et al., 1959; Green & Arduni, 1954) such that it appears to be functioning at a much lower level of arousal--as demonstrated in non-humans. 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, in order to monitor what is being received and processed, functions at a level much lower in order 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 in to information that is being processed at a low level of intensity.

Hence, in situations where both the cortex and the hippocampus become desynchronized, there results distractability and hyperresponsiveness such that the subject becomes overwhelmed, confused, and may orient to and approach several stimuli (Grastyan et al., 1959). Attention, learning, and memory functioning are decreased. Situations such as this sometimes also occur when individuals are highly anxious or repetitively emotionally or physically traumatized (see chapter 30).

The hippocampus consists of 3 layers, layer 2 consisting of pyramidal neurons which provide excitatory output and thus act to activate and arouse target tissues; via the transmitters glutamate and aspartic acid. In addition, the entorhinal cortex provides excitatory input into the hippocampus--input which is derived from the neocortex; using again, aspartic and glutamate acid (reviewed in Gloor, 1997). Specifically, it appears that the hippocampus interacts with the neocortex is regard to arousal via the dorsal medial nucleus of the thalamus, the septal nuclei, the hypothalamus, amygdala and brainstem--structures with which it maintains direct interconnections. As per the neocortex, this sheet of tissue is also innervated by these structures, and by the entorhinal cortex.

Hence, the hippocampus serves as a major component of an excitatory interface and can be aroused by neocortical activity (via the entorhinal cortex), and can provide excitatory input to directly to subcortical structures and indirectly to the neocortex (via the entorhinal cortex and dorsal medial nucleus). However, if the neocortex becomes excessively aroused, so to might the hippocampus, and vice versa. Under excessively arousing conditions, however, hippocampal pyramidal neurons may become inhibited or even damaged (Lupien & McEwen, 1997; Sapolsky, 1996), thus resulting in loss of memory.

There is also evidence to suggest that the hippocampus may act so as 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 is dampened (Feldman, 1962; Redding, 1967). On the otherhard, if cortical arousal is at a low level, hippocampal stimulation often results in an augmentation of the cortical evoked potential (Redding, 1967).

The hippocampus also exerts desynchronizing or synchronizing influences on various thalamic nuclei (e.g., the dorsal medial thalamus) which in turn augments or decreases activity in this region (Green & Adey, 1956; Guillary, 1955; Nauta, 1956, 1958). As the dorsal medial thalamus is the major relay nucleus to the neocortex, the hippocampus therefore appears able to block or enhance information transfer to various neocortical areas (that is, in conjunction with the frontal lobe, see chapter 19). Indeed, it may be acting to insure that certain percepts are stored in memory at the level of the neocortex (Gloor, 1997; Squire 1992) by modulating cortical activity.

It is thus likely that the hippocampus may act to influence information reception and storage at the neocortical level as well as possibly reduce extremes in cortical arousal (be they too low or high) perhaps by activating inhibitory circuits in the dorsal medial nucleus, thus ensuring that the neocortex is not over or underwhelmed when engaged in the reception and processing of information. This is an important attribute since very high or very low states of excitation are incompatible with alertness and selective attention as well as the ability to learn and retain information (Joseph et al. 1981; Lupien & McEwen, 1997; Sapolsky, 1996).

Aversion & 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 also prevent extremes in emotional arousal and thus maintain a state of quiet alertness (or quiescence). Moreover, similar to the results following stimulation of 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 mild punishment (Gray, 1970, 1990), particularly in regard to single trial but not multiple trial learning. For example, the hippocampus responds with trains of slow theta waves when presented with noxious stimuli but habituates or ceases to respond with repeated presentation. It is likely, however, that these physiological responses are secondary to activity within the amygdala and hypothalamus which then effects hippocampal functioning.


The hippocampus participates in the elicitation of orienting reactions and the maintainance of an aroused state of attention (Foreman & Stevens, 1987; Grastayan et al., 1959; Green & Arduini, 1954; Nishitani, et al., 1999; 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 seconds between bar presses if first trained to respond to a continous schedule. There is an inability to switch from a continous to a discontinous 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, et al. 1964). Habituation is largely abolished and the ability to think or respond divergently is disrupted. Disinhibition due to hippocampal damage can even prevent the learning of a passive avoidance task, such as simple ceasing to move (Kimura, 1958).

Hence, when coupled with the evidence presented above, it appears that the hippocampus acts to possibly selectively enhance or diminish areas of neural excitation which in turn allows for differential selective attention and differential responding, as well as the storage and consolidation of information into long term memory. 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.


The hippocampus is most usually associated with learning and memory encoding, e.g. long term storage and retrieval of newly learned information (Enbert & Bonhoeffer, 1999; Fedio & Van Buren, 1974; Frisk & Milner, 1990; Milner, 1966; 1970; Nunn et al., 1999; Penfield & Milner, 1958; Rawlins, 1985; Scoville & Milner, 1957; Squire, 1992; Victor & Agamanolis, 1990) particularly the anterior regions. Hence, if the hippocampus has been damaged the ability to convert short term memories into long term memories (i.e. anterograde amnesia), becomes significantly impaired in humans (MacKinnon & Squire, 1989; Nunn et al., 1999; Squire, 1992; Victor & Agamanolis, 1990) as well as primates (Zola-Morgan & Squire, 1984, 1985a, 1986). In humans, memory for words, passages, conversations, and written material is also significantly impacted, particularly with left hippocampal destruction (Frisk & Milner, 1990; Squire, 1992).

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 individual 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 (actually a few years before his surgery) he suffers the same grief as if he had just been informed for the first time.

H.M., although without memory for new (non-motor) information, 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" (Blakemore, 1977, p.96).

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 there results input overload, 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 attented 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).


The septal nuclei consists of medial and lateral nuclei, and can be further subdivided into several nuclear components (Ariens Kappers et al., 1936; Swanson & Cowan, 1979), such as the nucleus of the diagonal band of Broca. The septal nuclei is an evolutionary derivative of the hippocampus and the hypothalamus, and in the human brain is richly interconnected with both structures including the amygdala, and the substantia innomminata (SI) which is a major memory center, and which manufactures ACh--a transmitter directly implicated in memory (Gage et al., 1983; Olton, 1990). Andy and Stephan (1968) and Swanson and Cowan (1979) considered the bed nucleus of the stria terminals (which gives rise to a major pathway linking the septal nuclei, and amygdala and hypothalamus) as part of the septal nuclei, whereas others (Gloor, 1997) consider it to be part of the "extended amygdala." Likewise, some consider the nucleus accumbens as part of the septal nuclei, and others consider it part of the "extended amygdala;" i.e. the limbic striatum.

As noted the septal nuclei is massively interconnected with the hippocampus as well as with the entorhinal cortex (Swanson & Cowan, 1979) via a number of pathways, including the fornix. Directly implicating the septal nuclei in the memory functioning of the hippocampus is the finding that septal activation of this structure results in ACh secretion (Gage et al., 1983), whereas septal grafts into the hippocampus improves learning and memory (Gage et al., 1986). Conversely, lesions of the fimbria-fornix septal-hippocampal pathway results ACh depletion throughout the hippocampus (Gage et al., 1983; Olton, 1990), as well as loss of norepinephrine and serotonin coupled with memory loss (Olton, 1990).

The septal nucleus in part regulate hippocampal memory-related activity not only by stimulating ACh and other neurotransmitter production (Gage et al., 1983, 1986), but as it provides excitatory input and inhibitory-GABAnergic-- especially from the medial septal nuclei which in general exerts inhibitory influences not only on the hippocampus but the amygdala and hypothalamus. In general, it is supposed that the excitatory-inhibitory influences on the hippocampus (like those on the amygdala and hypothalamus) serve to modulate activity and prevent extremes in arousal (Joseph, 1992a, 1998b, 1999d). This is accomplished in part not only through the interconnections maintained with the amygdala, hypothalamus and entorhinal cortex, but the brainstem reticular formation (Petsche et al., 1965)--with which the hippocampus is also connected directly and via the entorhinal cortex.

Septal influences on hippocampal/entorhinal arousal is also indicated by fluctuations in rhythmic slow activity (theta), which is generated by both the hippocampus and entorhinal cortex (Alonso & Garcia-Austt, 1987). As detailed in chapter 14, theta is an indication of hippocampal arousal (Green & Arduini, 1954; Petsche et al., 1965; Vanderwolf, 1992) and is associated with learning and memory (O'Keefe & Nadel, 1978). Theta is a robust electrophysiological phenomenon which has been found in the hippocampus of most species studied, including monkeys (Stewart & Fxx, 1990) and humans (Sano et al., 1970); though in primates it seems to differ from the theta rhythm of non-primates (see Gloor, 1997).

O'Keefe and Nadel (1978) believe that theta plays an important role in creating the spatial maps that are maintained by hippocampal "place" neurons; i.e. pyramidal neurons which are attuned to specific environmental features and landmarks and the animals place in that environment as they move about. Moreover, long term potentiation (LTP) which is associated with learning and memory, is generated in those neurons demonstrating theta or activity that is at the "theta frequency" (Staubli & Lynch, 1987).

Neurons of the septal nucleus which innervate the hippocampus fluctuate in activity in parallel with changes in the theta rhythm (Petsche et al., 1965), whereas septal lesions abolish hippocampal theta (Green & Arduini, 1954). It has long been believed that septal neurons act as an interface between the reticular formation and the hippocampus (Petsche et al., 1965) and in conjunction with its connections with the amygdala and hypothalamus, therefore modulate hippocampal arousal as well as learning and memory.


It has been argued that significant impairments involving short-term memory and motor learning, cannot be produced by lesions supposedly restricted to the hippocampus (Horel, 1978; see also commentary in Eichenbaum et al. 1994); though in fact it is impossible to create such "restricted" lesions. Nevetheless, ignoring for the moment that inconvenient fact, in some instances with supposed restricted lesions, good recall of new information is possible for at least several minutes (Horel, 1978; Penfield & Milner, 1958; Squire 1992).

Moreover, there is considerable evidence which strongly suggests that the hippocampus plays an interdependent role with the amygdala in regard to memory (Gloor 1992, 1997; Halgren 1992; Kesner & Andrus, 1982; Mishkin, 1978; Murray 1992; Sarter & Markowitsch, 1985); particularly in that they are richly interconnected, merge at the uncus, and exert mutual excitatory influences on one another. For example, it appears that the amygdala is responsible for storing the emotional aspects and personal reactions to events in memory, whereas the hippocampus acts to store the cognitive, visual, and contextual variables (chapter 14) whereas that the amygdala activates the hippocampus by providing excitatory input (Gloor, 1955, 1997).

Specifically, the amygdala plays a particularly important role in memory and learning when activities are related to reward and emotional arousal (Gaffan 1992; Gloor 1992, 1997; Halgren 1992; LeDoux 1992, 1996; Kesner 1992; Rolls 1992; Sarter & Markowitsch, 1985). Thus, if some event is associated with positive or negative emotional states it is more likely to be learned and remembered.

The amygdala becomes particularly active when recalling personal and emotional memories (Halgren, 1992; Heath, 1964; Penfield & Perot, 1963), and in response to cognitive and context determined stimuli regardless of their specific emotional qualities (Halgren, 1992). However, once these emotional memories are formed, it sometimes requires the specific emotional or associated visual context to trigger their recall (Rolls, 1992; Halgren, 1992). If those cues are not provided or ceased to be available, the original memory may not be triggered and may appear to be forgotten or repressed. However, even emotional context can trigger memory (see also Halgren, 1992) in the absence of specific cognitive cues.

Similarly, it is also possible for emotional and non-emotional memories to be activated in the absence of active search and retrieval, and thus without hippocampal or frontal lobe participation. Recognition memory which may be triggered by contextual or emotional cues. Indeed, there are a small group of neurons in the amygdala, as well as a larger group in the inferior temporal lobe which are involved in recognition memory (Murray, 1992; Rolls, 1992). Because of amygdaloid sensitivity to visual and emotional cues, even long forgotten memories may be evoked via recognition, even when search and retrieval repeatedly fail to activate the relevant memory store.

According to Gloor (1992), "a perceptual experience similar to a previous one can through activation of the isocortical population involved in the original experience recreate the entire matrix which corresponds to it and call forth the memory of the original event and an appropriate affective response through the activation of amygdaloid neurons." This can occur "at a relatively non-cognitive (affective) level, and thus lead to full or partial recall of the original perceptual message associated with the appropriate affect."

In this regard, it appears that the amygdala is responsible for emotional memory formation whereas the hippocampus is concerned with storing verbal-visual-spatial and contextual details in memory. Thus, in rats and primates damage to the hippocampus can impair retention of context, and contextual fear conditioning, but it has no effect on the retention of the fear itself or the fear reaction to the original cue (Kim & Fanselow 1992; Phillips & LeDoux 1992, 1996; Rudy & Morledge 1994). In these instances, fear-memory is retained due to preservation of the amygdala. However, when both the amygdala and hippocampus are damaged, striking and profound disturbances in memory functioning result (Kesner & Andrus, 1982; Mishkin, 1978).

Therefore, the role of the amygdala in memory and learning seems to involve activities related to reward, orientation, and attention, as well as emotional arousal and social-emotional recognition (Gloor, 1992, 1997; Rolls, 1992; Sarter & Markowitsch, 1985). If some event is associated with positive or negative emotional states it is more likely to be learned and remembered. That is, reward increases the probability of attention being paid to a particular stimulus or consequence as a function of its association with reinforcement (Gaffan 1992; Douglas, 1967; Kesner & Andrus, 1982).

Moreover, the amygdala appears to reinforce and maintain hippocampal activity via the identification of motivationally significant information and the generation of pleasurable rewards (through action on the lateral hypothalamus). However, the amygdala and hippocampus act differentially in regard to the effects of positive vs. negative reinforcement on learning and memory, particularly when highly stressed or repetitively aroused in a negative fashion. For example, whereas the hippocampus produces theta in response to noxious stimuli the amygdala increases its activity following the reception of a reward (Norton, 1970).


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 constrasted with individuals with right sided destruction. Left sided damage disrupts the ability to recall simple sentences, complex verbal narrative passages, or to learn verbal paired-associates or a series of digits (Frisk & Milner 1990; Milner, 1966, 1970, 1971; Squire 1992).

In contract, right temporal destruction typically produces deficits involving visual memory, such as the learning and recall of geometic patterns, visual or tactile mazes, locations, objects, emotional sounds, or human faces (Corkin, 1965; Milner, 1965; Nunn et al., 1999; Kimura, 1963). Right sided damage also disrupts the ability to recognize (via recall) olfactory stimuli (Rausch et al. 1977), or recall emotional passages or personal memories (Cimino et al., 1991; Wechsler, 1973).

It appears, therefore, that the left amygdala and hippocampus are 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 non-verbal, visual-spatial, environmental, emotional, motivational, tactile, olfactory, and facial information. These issues and the differing roles of these nuclei in memory formation, as well as amnesia and repression will be discussed in greater detail in chapters 29, 30.


The amygdala maintains a functionally interdependent relationship with the hypothalamus in regard to emotional, sexual, autonomic, consumatory and motivational concerns. It is able to modulate and even control rudimentary emotional forces governed by the hypothalamic nucleus. However, the amygdala also acts at the behest of hypothalamically induced drives. For example, if certain nutritional requirements need to be meet, the hypothalamus signals the amygdala which then surveys the external environment for something good to eat (Joseph, 1982, 1992a). On the otherhard, if the amygdala via environmental surveilance were to discover a potentially threatening stimulus, it acts to excite and drive the hypothalamus as well as the basal ganglia so that the organism is mobilized to take appropriate action. 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 so that certain ends may be attained (Joseph, 1982, 1992a)


The amygdal-hippocampal complex, particularly that of the right hemisphere, is very important in the production and recollection of non-linguistic and verbal-emotional images associated with past experience. In fact direct electrical stimulation of the temporal lobes, hippocampus and particularly the amygdala (Gloor, 1990, 1997) not only results in the recollection of images, but in the creation of fully formed visual and auditory hallucinations (Gloor 1992, 1997; Halgren 1992; Halgren et al., 1978; Horowitz et al., 1968; Malh et al., 1964; Penfield & Perot, 1963), as well as feelings of familiarity (e.g. deja vu).

Indeed, it has long been know that tumors invading specific regions of the brain can trigger the formation of hallucinations which 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; Gloor 1992, 1997; Halgren 1992; 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 (Gloor 1992, 1997; Halgren 1992; 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 complex visual hallucinations, body sensations, deja vus, illusions, as well as gustatory and alimentary experiences (Weingarten et al. 1977), whereas Freeman and Williams (1963) have 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 memory- and dream-like hallucinations (Halgren et al. 1978; Horowitz et al. 1968).

The amygdala also becomes activated in response to bizarre stimuli (Halgren, 1992). Conversely, if activated to an abnormal degree, it may in turn produce bizarre memories and abnormal perceptual experiences. In fact, the amygdala contributes in large part to the production of very sexual as well as bizarre, unusual and fearful memories and mental phenomenon including dissociative states, feelings of depersonalization, and hallucinogenic and dream-like recollections (Bear, 1979; Gloor, 1986, 1992, 1997; Horowitz et al. 1968; Mesulam, 1981; Penfield & Perot, 1963; Weingarten et al. 1977; Williams, 1956).

In addition, sexual feelings and related activity and behavior are often evoked by amygdala stimulation and temporal lobe seizures (Halgren, 1992; Jacome, et al. 1980; Gloor, 1986, 1997; Remillard, et al. 1983; Robinson & Mishkin, 1968; Shealy & Peele, 1957), including memories of sexual intercourse (Gloor 1990) or severe emotional trauma and abuse (Gloor, 1997).

Moreover, intense activation of the temporal lobe and amygdala has been reported to give rise to a host of sexual, religious and spiritual experiences; and chronic hyperstimulation (i.e. seizure activity) can induce some individuals to become hyper-religious or visualize and experience ghosts, demons, angels, and even God, as well as claim demonic and angelic possession or the sensation of having left their body (Bear 1979; Gloor 1986, 1992; Horowitz, Adams & Rutkin 1968; MacLean 1990; Mesulam 1981; Penfield & Perot 1963; Schenk, & Bear 1981; Weingarten, et al. 1977; Williams 1956).


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 occurs in the hippocampus and amygdala (Chapman & Walter, 1965; Chapman et al. 1963), but with little cortical abnormal activity. In both humans and chimps, when the temporal lobes, amygdala and hippocampus are removed, LSD ceased to produce hallucinatory phenomena (Baldwin et al. 1959; Serafintides, 1965). Moreover, LSD induced hallucinations are significantly reduced when the right vs. left temporal lobe has been surgically ablated (Serafintides, 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 which acts to interpret this material (Penfield & Perot, 1963) as perceptual phenomena. Indeed, it is the interrelated activity of the temporal lobes, hippocampus and amygdala which not only produce memories and hallucinations, but dreams. In fact, the amygdalas involvement in all aspects of emotion and sexual functioning, including associated memories, the production of overwhelming fear as well as bizarre and dream-like mental phenomenon, may well account for why this type of unusual stimuli, including personal and innocuous memories also appears in dreams.


When hallucinations follow depth electrode or cortical stimulation, much of the material experienced is very dream-like (Gloor 1990, 1992; Halgren et al., 1978; Malh et al., 1964; Penfield & Perot 1963) and consists of recent perceptions, ideas, feelings, and other emotions which are similarly illusionary and dream-like. Indeed, the right amygdala, hippocampus, and the right hemisphere in general (Broughton, 1982; Goldstein et al., 1972; Hodoba, 1986; Humphrey & Zangwill, 1961; Kerr & Foulkes, 1978; Meyer et al. 1987) also appear to be involved in the production of deam imagery as well as REM sleep (chapter 10).

For example stimulation of the amygdala triggers and increases ponto-geniculo-occipital paradoxical activity during sleep (Calvo, et al. 1987), which in turn is associated with REM and dreaming. In addition, during REM, the hippocampus begins to produce slow wave, theta activity (Jouvet, 1967; Olmstead, Best, & Mays, 1973; Robinson et al. 1977), which is associated with long-term potentiation which is associated with learning and memory (see chapter 14).

Presumably, during REM, the hippocampus and amygdala act as a reservoir from which various images, emotions, words, and ideas are drawn and incorporated into the matrix of dream-like activity being woven by the right hemisphere. It is probably just as likely that the right hippocampus and amygdala serve as a source from which material is drawn during the course of a daydream.

The Right Hemisphere & Dreams.

There have been reports of patients with right cerebral damage, hypoplasia and abnormalities in the corpus callosum who have ceased dreaming altogether, suffer a loss of hypnogic imagery or tend to dream only in words (Botez et al. 1985; Humphrey & Zangwill, 1951; Kerr & Foulkes, 1981; Murri et al. 1984). However, there have also been some report 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 N-REM (Goldstein et al. 1972; Hodoba, 1986). Similarly, measurements of cerebral blood flow have shown an increase in the right temporal regions during REM sleep and in subjects who upon wakening report visual, hypnagogic, hallucinatory and auditory dreaming (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). Hence, it appears that there is a specific complementary relationship between REM sleep and right temporal electrophysiological activity.

Interestingly, daydreams appear to follow the same 90-120 minute 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 hemisphere tend to oscillate in activity every 90-120 minutes -- a cycle which appears to correspond to the REM-NREM cycle and the appearance of day and night dreams. Forgotten Dreams.

Most individuals, however, have difficulty recalling their dreams. This may seem paradoxical considering that hippocampal theta is being produced. However, this is theta punctuated by high levels of desychronized activity, which is not conducive to learning. In this regard, theta activity may represent the reverberating activity of neural circuits formed during the day, such that the residue of day time memories come to be inserted into the dream. Conversely, due to the high level of desychronization occuring in the hippocampus (as it is so highly aroused), although it contributes images and the days memories, it does not participate in storing these dream-like experiences into memory.

Consider the results from temporal lobe, amygdala, and hippocampal electrical stimulation on memory recall and the production of hallucinations. Although personal memories are often activated at low intensities of stimulation (memories which are verified not only by the patient but family), if stimulation is sufficiently intense, the memory instead will become dreamlike and populated by hallucinated and cartoon like characters (Halgren, et al. 1978). That is, at low levels of stimulation memories are triggered but these memories become increasingly dream-like with high levels of activity. Moreover, once these high levels of stimulation are terminated, patients soon become verbally amnesic and fail to verbally recall having had these experiences (Gloor, 1992; Horowitz, et al. 1968).

However, these memories can be later recalled if subjects are provided with specific contextual cues (Horowitz, et al. 1968). The same can occur during the course of the day when a fragment of a conversation, or some other experience, suddenly triggers the recall of a dream from the previous night which had otherwise been completely forgotten. Presumably it had seemingly been forgotten because the hippocampus did not participate in their storage and thus could not assist in their retrieval (see chapters 29, 20).

There is also some evidence to suggest that different regions of the hippocampus show different levels of arousal during paradoxical sleep. For example, it appears that the posterior hippocampus becomes activated during paradoxical sleep and shows theta activity, whereas the more anterior portions become inhibited (Olmstead et al. 1973). As the anterior portions are more involved in new learning (at least in humans), whereas the posterior hippocampus is more concerned with old and well established memories, this would suggest that the posterior hippocampus is contributing older or already established memories to the content of the dream--which explains why theta, which is associated with learning and memory, is also produced during the dream--that is, it is replaying various fragmentary memories. Conversely, the inhibition of the anterior region would prevent this dream material from becoming rememorized.


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; Parmelee et al. 1967). Among infants, however, REM occur during wakefullness 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. 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 dream-like state. Possibly, this state corresponds to what Freud has 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 which occurs while eating or sucking may have to do with the limbic structures which are involved not only in the production of dream-like activity, but the identification, learning and retention of motivationally significant information (i.e. the amygdala and hippocampus).

Presumably this relationship is a consequence of REM as well as eating and sucking being mediated, in part, by the amygdala as well as other limbic nuclei, which are also concerned with forming motivationally significant memories. Hence, when hungry, the hypothalamus becomes aroused which activates the amygdala which is responsible for the performing environmental surveillance so as to attend, orient to, identify and approach motivationally significant stimuli and eat. However, because the infants brain is so immature and as its resources for meeting its limbic needs are quite rudimentary, under certain conditions prolonged hypothalamus induced amygdala activation results in the formation and recall of relevant memories which may be experienced as hallucinations of the desired object. That is, previously formed neural networks become activated and the infant begins to dream and hallucinate food and will then suck and smack its lips as if eating or sucking when it is awake, in REM, and there is no food present.


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 slacking this desire. The hypothalamus can only say: "I want", "I need", and can only signal pleasure and displeasure. However, being 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.

Nevertheless, the cry does not produce the immediately desire relief or reduction in tension. There is thus a pressure 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 hippocampus develop, the organism begins to develop an eye that not only sees outward, but which can register and recall events, objects, people, etc., associated with tension reduction, pleasure and the satiaty of the infants internal needs (e.g. the taste, smell, feeling of mother's breast and milk, the experience of sucking and relief, etc.). 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.


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 "prgorams" are formed which correspond to the repeated registration of experiences which are deemed significant (e.g. pleasurable). That is, neural pathways which 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 (chapter 14); i.e. a memory is created. Eventually, if this circuit is reactivated, the "learned" pattern is reexperienced; i.e. the organism remembers.

Thus, infants as young as 2 days of age can learn to suck at the mere sight of a bottle (see Piaget, 1954) and in order to receive milk as a reinforcement, infants can even modify their sucking response (Sameroff & Cameron, 1979). Hence, they are suceptible to classical conditioning (Sameroff & Cavanagh, 1979), although the possibility of operant conditioning has not been established. Nevertheless, the fact that they can recognize the bottle and suck (as well as cry and shed tears) indicates that various regions of the limbic system, especially that of the amygdala is functional and that learning and the creation of specific, context specific neural circuits have been formed very early in life.

Thus, when the amygdala/hippocampus are stimulated by a hungry hypothalamus, the events and images associated with past experiences of pleasure can not only be searched out externally, but recalled in imaginal form. For example, as an infant experiences hunger and stomach contractions as well as it own cries of displeasure, these states become associated with the sound, smell, taste, etc. of mother and her associated movement and other stimuli which 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 and the creation of a specific neural network subserving that memory (chapter 14).

Eventually, when the infant becomes hungry, if prolonged there is the possibility that the entire neural sequence associated with hunger and feeding (i.e. hunger, mother, food, satiaty), may become involuntarily triggered and activated (via association) such that an "image" of being fed is experienced. The activation of these rudimentary and infantile memory-images is probably what consititutes, at least in part, the primary process.

Behaviorally this is manifested by REM and via sucking and tongue movements as if eating, when in fact there is no food present (cf, Piaget, 1952). That is, when hungry, the infant will begin to cry, rapid eye movement (REM) might be observed, and then the infant will stop crying and smack its lips and make sucking movement (mediated by the amygdala) as if it were being fed. The infant experiences the experience of being fed in the form of a dream (Joseph, 1982) or hallucination, although it is awake.

In that the brain of the human infant is quite immature for in fact several years, which in turn restricts information reception and processing (chapters 23-28), and given the limited amount of reality contact infants are able to achieve, these rudimentary memories and images (even when occurring during waking, i.e. REM), are probably indistinguishable from actual experience simply because they are experience.

Like a dream, when replayed, the infant presumaly reexperiences to some degree the sensations, emotions, etc., originally linked to tension reduction. Thus, the young infant, as yet unable to distinguish between representation and reality, responds to the image as reality (Freud, 1900, 1911), even while awake--as manifested by REM. When hunger is prolonged the association linked to feeding are triggered and for a brief time 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 (Nakamuar & 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.

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