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Brain

mechanisms

of emotion

and emotional

learning

Joseph E. LeDoux
New York

The

amygdala

emotional

University,

appears

information

to

play

processing

New York,

New York,

an

role

have begun to clarify the anatomical
contribution
emotional
circuits

of its individual
learning

involved

between
subcortical

and

memory.

regions,

subregions,

of sensory

functions,

can now point
inputs

and to efferent

for specific emotional

many

aspects

of the ainygdala

to emotional

Researchers

in

of

Studies over the past year

organization

subregions

in the transmission

amygdaloid

essential

and behavior.

USA

and the
especially

to plausible

into the amygdala,

targets

in cortical

and

-,

learning and memory processes.
-;.

.:

I.

-

.I

L,
A

Current

Opinion

in Neurobiology

Introduction

in emotional
memory.

Research over the past 40 years has pointed to the amygdala as the heart and soul of the brain’s emotional network [l-5,6=*,7**]. Following Kluver and Bucy’s [8] ohservation that damage to the temporal lobe in monkeys
produced a variety of emotional disturbances, Weiskrantz
[9] demonstrated
that damage to the amygdala alone
would also produce the syndrome.
Subsequently,
the
amygdala has been implicated in essentially every experimental task that has been used to study emotional representation in the brain. No other brain area has been
so consistently implicated in emotional processes [lo**].
Although the amygdala is not the only structure involved
in emotion (see [ 11,12]), and emotion is not the only
function of the amygdala (see [ 13**] ), the amygdala is an
essential component of the brain’s emotional system. The
following brief review of research during the past year
concerned with the brain mechanisms
of emotion will
the&fore concentrate on the contribution
of the amygdala to emotional processes.

In spite of the clear involvement of the amygdala in emotional functions, until recently little progress had been
made in understanding
the functional organization of the
amygdala in emotion. In the older anatomical literature
the amygdala was divided into two general subareas, the
basolateral and the cortico-medial
groups. Today, the
amygdala is generally conceived in a far richer fashion,
often being divided into as many as ten or more subareas,
each with its own subdivisions and unique sets of affer
ent and effejent connections
[14,15]. It is unlikely that
emotion is mediated by the amygdala acting as a whole,
or even as a two-part collection of nuclei, and it is neces
sary to isolate the contribution
of individual subareas to
different aspects of emotional functions. The emphasis of
this review will therefore be on recent advances in our
understanding
of the anatomical organization of individual amygdaloid subareas and the role of these subareas

,,

1992, 2:191-197

Anatomical

functions,

especially emotional

organization

learning

and

of the amygdala

The emotional functions of the amygdala critically depend upon the reception of sensory inputs. Many of
the sensory projections
to the amygdala terminate in
the lateral amygdaloid nucleus. These projections
originate mainly in the sensory processing areas of the cortex and thalamus. While the cortico-amygdala
projections had been well characterized
at the light microscopic level [14,16,17], much less was known about the
thalamoamygdala
projections.
Recent studies by my colleagues and I have shown that
the auditory projection to the lateral amygdala from the
thalamus originates primarily in the posterior intralaminar nucleus, a thalamic cell group that receives auditory
inputs from the inferior colliculus and is associated with
the medial geniculate body (Fig. 1) [ 181. About half of
the thalamo-amygdala
projection neurons in this region
can be labeled with an antibody against glutamate, suggesting that neural transmission
in this pathway may be
mediated by this excitatory amino acid transmitter subthe synaptic profile of these
stance [ 19**]. Furthermore,
terminals [ 20**] is similar to that of glutamate-containing
terminals in this region (CR Farb and JE LeDoux, unpublished data). The above studies provide the most detailed
understanding
to date of the morphology of any sensory
projection to the amygdala.
Sensory transmission to the amygdala from the thalamus
is not limited to the auditory modality. An extensive study
of thalamwamygdala
projections across sensory modalities has been carried out by Turner and Herkenham
[21**]. Radiolabeled
amino acids were injected into various thalamic nuclei and transport to the amygdala was

Abbreviations
LTP-long-term

potentiation; NMDA-N-methyl-o-aspartic

acid; Pha-L-fhaseolus

@ Current Biology Ltd ISSN 0959-4388

vulgaris leucoagglutinin
191

While MGv only projects to primary auditory cortex. which synapse in the ventral division of the medial geniculate body (M&I. which projects widely to corttcal areas (not shown) and to the central nucleus of the amygdala (ACE).13-]. as well as to the lateral nucleus of the amygdala (AL). contains glutamate (Clu). Thalamo-amygdala projections have been implicated in emotional learning. when activated directly by sensory projections from the ventral thalamus. Cholinergic transmission to the cortex from the nucleus basalis has been implicated in cortical arousal and plasticity. however. including the medial division of the medial geniculate body (MCm) and the posterior intralaminar nucleus (PIN). . which projects widely to cortical areas. gave rise to emotional behavior by way of projections to the brainstem and gave rise to subjective emotional experiences by way of projections to the cerebral cortex. Their findings show that the amygdala receives subcortical inputs from a wide variety of sensory systems. Extralemniscal pathways transmit to other parts of the auditory thalamus. The thalamo-amygdala projection forms asymmetric. which may be important in certain emotional situations. These theories suggested that the hypothalamus. The classic theories of Cannon [22]. and may use this excitatory substance as a neurotransmitter.7-. Bard [23] and Papez [24]. and high-frequency stimulation of these projections produces long-term potentiation (LTP) in AL. emphasized the importance of subcortical sen sot-y transmission in the experience and expression of emotion. Direct projections to the amygdala have not figured prominently in contemporary thought about the neural basis of emotion. Thalamic inputs to the amygdala allow sensory signals to activate it either before or simulta neous with the arrival of signals at the cortical level. A diagram illustrating some of the pathways underlying emotional informatton processing and response control by the amygdala. The pathway from the nucleus basalis to cortex uses acetylcholine (ACh) as a neurotransmitter. Because these projections exit the primary sensory systems at an early stage of processing. however. especially fear conditioning (see [6**] ). ThalamWamygdala projections have been implicated in emotional learning processes. MCmiPlN projects to both primary and association areas of auditory cortex. Pathways through which auditory inputs are transmitted to the amygdala are shown but similar circuits also exist for other sensory systems. they are unlikely to encode complex stimulus representations. These pathways are also involved in emotional learning and exhibit LTP. They may allow primitive sensory representations to rapidly activate the amygdala. and may therefore play an important role in preconscious and precognitive emotional processing. Auditory and polymodal association areas relay auditory signals to AL by way of the external capsule. The finding of extensive subcortical sensory innervation of the amygdala by thalamic projections fits well with the spirit of these theories. Tonotopically organized auditory signals are transmitted to the auditory thalamus over lemniscal pathways. which tends to focus on corticcramygdala systems [l-5. It also projects to the nucleus basalis. excitatory (+ 1 contacts with AL. AL projects to the basolateral nucleus of the amygdala (ABL). 1. ACE has extensive connectivity with brainstem areas involved in the control of emotional responses.192 Cognitive neuroscience Arousal and plasticity Behavioral Lemniscal auditory pathways Extralemniscal auditory pathways Emotional Autonomic response Endocrine control systems Fig. examined.

and small lesions of other subregions of the amygdala. most of the sensoty projections to the amygdala terminate in the lateral amygdaloid nucleus. particula@ . and later extended to several other response modalities [30. as described below. connections from this nucleus to other amygdaloid regions must play an important role in the emotional processing functions of the amygdala. Graham and Holland [35**] show that it is also involved in appetitive conditioning. Until recently it had been technically cumbersome to study the intrinsic organization of the amygd&. Recent studies by Gallagher. lesions that completely destroyed the lateral nucleus at a designated level of the amygdala. Thus. they found that central nucleus lesions selectively impaired conditioned-stimulus related responses. versus Our knowledge of anatomical interactions between thalamwamygdala and corticcl-amygdala connections is in its infancy. the two projection systems overlap and may in fact converge in the lateral nucleus [25-l.conditioned place preference learning in rodents [33**. These observations are of significance for several reasons. CR Farb. The central nucleus of the amygdala is not exclusively involved in aversive emotional learning. Lesions of the lateral/basolateral amygdala interfere with the formation of these conditioned place preferences. Thus. Conditioned place preferences are established by providing reinforcing stimulation in a certain location. This can be done with either primary reinforcers (such as desirable foods) or by chemical or electrical brain stimulation. IJsing a task which separates out conditioned responses related to the conditioned stimulus. such as ‘freezing’ and changes in autonomic activity.e. the lateral nucleus of the amygdala. The lateral nucleus has also been it?ipli&@ . The effect of the lesions appears to involve the interruption of the flow of sensory information from the lateral/basolateral region to the nucleus accumbens. unlike the lateral nucleus. Given that much of the sensory ctierentation of the amygdala is by way of the lateral nucleus. This kind of behavioral analysis has not yet been performed for other conditioning paradigms. is paired with a footshock [ 281. It might be expected that lesions of this structure would disconnect the amygdala from environmental information and therefore reproduce the disruptive effects on emotional functions of both large amygdaloid lesions. First. and would place the lateral nucleus of the amygdala in a key position to coordinate the flow of sensory information that ultimately leads to emotional reactions. but progress in this area is essential for understanding how the amygdala integrates diverse sensory inputs in emotional information processing. electrical stimulation of the central nucleus produces cortical electroencephalogram desynchroniza- 193 . Functional specialization within the amygdala As described above. Sensory information reaching the lateral nucleus from either cortex or thalamus can thus influence on-going cortical processing by way of the lateral to basolateral projections. is believed to play an important role in the expression of behavioral and autonomic responses associated with emotional arousal. appears to be involved in both place preference formation and fear conditioning. The introduction of the Pbaseolus vulgaris leucoagglutinin (Pha-L) axonal transport neural tract-tracing method [ 261. and those related to the unconditioned stimulus. This notion was first demonstrated in studies of conditioned bradycardia by Kapp and coworkers [29]. Pittinen and Amaral [27**] placed injections of Pha-L into the lateral nucleus and demonstrated a previously unknown projection to the basolateral nucleus in primates. such as a tone. Studies in rats have confirmed the existence of this projection (JE Ledoux. provides a link by which sensor)i inputs to the lateral nucleus can activate emotional behaviors and autonomic responses. G Go.Brain even if the anatomical thalamo-hypothalamic details (thalamo-amygdala projections) are different. visualization of full axonal arborizations. a structure that is known to be necessary as an amygdaloid output in the expression of emotional responses [2!+3l].31]. One study of rodents involved classical fear conditioning. identification of cells involved in uptake and transport. where sensory information may normally be associated with reward information by interactions with dopamine containing terminals. Second. i. by virtue of its input from sensory processing structures. the basolateral nucleus projects heavily to the central nucleus of the amygdala [ 14.27-l. but seems to use different e&rent projections in these forms of learning. After several pairings the tone elicits emotional (fear) reactions. unpublished data). unlike the lateral nucleus. a procedure whereby an affectively neutral stimulus. has solved this problem and has provided some new insights into amygdala organization. which allows for the placement of very restricted injection sites.34*0]. Within a given sensory modality. involving several subregions (including the lateral nucleus). by way of its extensive connectivity with brainstem areas. and can influence cortical arousal. studies of non-human primates have shown that subtotal lesions of the amygdala that encroach upon the lateral nucleus produce the loss of fear and other components of the Kliiver-Rucy syndrome [32*-l. The central nucleus of the amygdala. and that did not encroach upon the central nucleus of the amygdala. The problem is that its subregions occupy small volumes and therefore it is diffkult to restrict the injection of tracer substances to one region. Similarly. and identification of synaptic boutons at the light microscopic level. Recent studies have in fact shown that lesions confined to the lateral nucleus produce the predicted ‘disconnection’ mechanisms of emotion and emotional learning LeDoux effects in several different behavioral tasks.in appetitive emotional reactions. Convergence would allow thalamic and cortical sensory inputs to act on common ensembles of amygdala neurons. place preferences appear to involve projections to the nucleus accumbens and fear conditioning involves projections to the central nucleus of the amygdala. L Steffanacci. A large sample size was necessary to generate a small group with acceptable lesions. which. the basolateral nucleus projects heavily to cortical association areas [14. More recent studies by Kapp’s group [36*-l have shown that the central nucleus also plays an important role in regulating the state of arousal of the neocortex. A Pitkanen and DG Amaral.151.

which involves an increase in the effcacy of synaptic transmission as a result of high frequency (tetanizing) stimulation of an afferent pathway. It is induced in pathways that are known to have clear roles in well characterized and specific learning processes. mediate these changes. Collectively. Thus. which also receives tierents from non-sensory association regions. even if corticcramygdala LTP turns out not to involve NMDA receptors. More specifically. and corticwamygdala projections (the external capsule) in vitro [46]. attentional. it is believed that connections from the central nucleus to the cholinergic neurons of the nucleus basalis. As this effect is abolished by systemic administration of the cholinergic antagonist atropine. Fourth. In the hippocampus. Future studies should determine which substances are used in normal transmission and synaptic plasticity by projections from individual cortical areas. memory. its implications for understanding synaptic plasticity in the amygdala should not be over interpreted at this point. Because of the important implications of this finding. although the observation that blockade of NMDA receptors in the lateral/basolateral amygddki fails to interfere with LTP is one of the most important findings of the past year. In some hippocampal pathways. It has also been shown that intraventricular injections of NMDA antagonists interfere with the acquisition presumably but not the expression of fear conditioning. thalamcl-amygdala transmission is not only essential for subcortical emotional learning and non-specific arousal (see above). which then projects to the nucleus basalis. which projects widely to cortex. If multiple mechanisms are involved in external capsule LTP. and thereby changes the strength of inputs of that frequency. these findings suaest that excitatory amino acid receptors in the amygdala may play a CrUCid role in synaptic transmission and synaptic plasticity in the sensory projections to the amygdala. it needs to be considered in some detail. suggests that synaptic plasticity in the amygdala is not mediated by NMDA receptors [49**]. the recordings were made in the lateral and basolateral nuclei. LTP is mediated by excitatory amino acid receptors [41-43]. given the diverse origins of the fibers stimulated. Selective tetanization of the individual cortical areas that project to the amygdala would be useful. Although the amygdh will always lack the convenient anatomical organization of the hippocampus. the study involved stimulation of the external capsule. The cortical inputs to the lateral and basolateral nuclei are very different. and pathway 2. Careful comparisons therefore need to be made between synaptic plasticity in the lateral versus basolateral areas. Several points should be noted. Like LTP. It is not known whether all or only some of the projections traveling through the external capsule are plastic. Regardless of the mechanism. and in emotional learning processing mediated through these projections. Cellular mechanisms of emotional learning in the amygdala It is widely believed that synaptic plasticity underlies the rapid induction of memories through experience (see [3%40]). Second. studies of amygdala LTP may help to uncover basic mechanisms through which normal and . the case would still be open with respect to thalamo-amygdala projections. the thalamo-amygdala projection to the nucleus basalis increases the postsynaptic excitability of pyramidal cells in auditory cortex (cells that receive the frequency-specific inputs from the ventral division of the medial geniculate body). amygdala LTP is extremely important. glutamate. an extralemniscal relay from the medial areas of the medial geniculate body to the amygdala. is present in the cells of origin of at least some sensory inputs to the lateral nucleus of the amygdala [ 19**]. One of the most extensively studied models of synaptic plasticity is long-term potentiation (LTP) [41-43]. First. Third. by acting in the amygdala [48-l. Further. LTP in some pathways is NMDA dependent while in others it is not. and that excitatory amino acid receptors are highly concentrated in the lateral/basolateral region [44]. however. but may also contribute to highly specific plastic modifications occurring in the cerebral cortex. Lesions of the lateral nucleus interfere with fear conditioning [28] and blockade of N-methyl-D-aspat-tic acid (NMDA) receptors in the lateral/basolateral amygdala interferes with the acquisition [47**] of fear conditioning.194 Cognitive neuroscience tion. A recent in vitro study of LTP. the stimulation conditions of LTP are similar to the stimulation conditions of the associative conditioning tasks that have been used to implicate the amygdakd in emotional learning and memory processes. It is thus significant that the excitatory amino acid. Kapp’s observations of an amygdala-mediated cholinergic arousal of cortex are in close accord with Weinberger’s [ 37**] recent suggestion that learning-induced changes in the receptive field functions of neurons in auditory cortex critically involve parallel transmission and convergence of two pathways: pathway one. the conditioned associations mediated by the amygdala are rapidly learned and long lasting. and other cognitive processes mediated at the neocortical level. This cholinergic arousal system may allow emotional information processing by the amygdala (particularly by the lateral-basolater&central connection) to influence perceptual. a specific (lemniscal) relay of tonotopic auditory information from the ventral division of the medial geniculate body to the auditory cortex. it is possible that NMDA and non-NMDA (and possibly even non-excitatory amino acid) mechanisms are involved in the overall effect. Thus. This close correspondence between LTP and behavior has been lacking for the hippocampus and has hindered progress in relating hippocampal LTP to real-life learning and memory phenomena. This area of work has just begun and much more work needs to be done. Furthermore. blockade of only the NMDA receptors would not completely block LTP. The lateral nucleus receives much of the direct sensory innervation from cortex and thalamus and then projects to the basolateral nucleus. which projects widely to the neocortex. LTP has been induced in the lateral/basolateral amygdala by stimulating thalameamygdala projections in ztizlo[45]. Weinberger proposes that pathway 2 enters into ‘Hebbian synapses’ with pathway 1 and as a result modifies the receptive fields of the involved neurons. which contains fibers from many areas of the neocortex.

It is the most thorough survey of the amygdala available toddy. 1985:223-334. ALIIEIII G.s S”slrm. and it is too early to conclude that the amygdala does not have an NMDA-mediated form of LTP.y&zla: Neurobiokgical Aspects ofEmotio?z. In ne Amygdaloid Comple. Beball Brain Sci 1982. LELXXIXJE. LEDOUX JE: Emotion and the AmygdaIa.. A thorough review of the involvement of the . and may also be useful as a model system for furthering our understanding of the relationship between LTP and memory. Conclusions The amygdala has long been viewed as playing an important role in emotion. New findings relating to the organization.353.. Bmo tion and Psychosomatic IlInes. The review points out certain discrepancies between findings from human and animal research. Amskxiam Elsevier. 119. Edited by Aggleton J. 1986. . AGCLET~NJP. there has been an explosion of research aimed at understanding the anatomical organization of this structure and its contribution to emotion. Acknowledgement Supported MH465IG. tion. HALGRFN E: Emotional Neurophysiology within the Context of Human Cognition. IX. LeDoux Y. Tokyo: Japan In The Am.Other Symptoms Following Bilateral TemporalZol&tom+ in Rhesus Monkeys.Brain mechanisms pathological emotional memories are formed. Edited by Aggleton J. KI. however. and may also contribute to cortical arousal and plasticity in emotional situations. Con10.TRAMINOC. Diversity and Sprouting of Cortical Projections to the Amygdala in the Rhesus Monkey. and Mental 0~1s~ function. In Physiology. FARISCR. New York: Wiley-L&. . J Neurosci 1990.2?2. J Camp Pbysiol ~sychol 1956. New York: WileyLiss. Memory. 2: 281-299. 1992. J Comp Neural 1980.. 1992. RI:GGIEKO DA: Topographic tion of Neurons in the Acoustic Thalamus that the Amygdala. EIXNGER Theory of H: Neural Control of Aggression and Rage In f~andbook of the tf@othalamus. an anatomical understanding of the input-output relations that underlie information processing by this structure. 5:21 l-294. Edited by Plum F. Neuroxt Lett 1991. 6. . 1960. . MBHKIN M.s of Emu Dysjunction. 1987.EL A. ROLLSET: A Theory of Emotion and its Application to Understanding the Neural Basis of Emotion. 10:1043-1054. Edited by Paxinos G.spects of Emotion. LEDorrx JE: Emotion. DEOLM~S J. 17. especially those concerned with how sensory inputs reach and are subsequently distributed throughout the amygdala. OrganizaProject to I~l)ol~x JE. Amygdala.~NER H. In ne &at Ner~otr. 7. WI. 1986: 325-344. have been especially helpful. counted for. In Handbook of Pbysioloff/. Kellerman H. AGGLE’I’ONJ: The Am&ala- . as they begin to provide. Although blockade of NMDA receptors in the amygdala does not interfere with LTP. in press. Orlando: Academic Press. Projections to the amygdala from sensory processing areas of the thalamus are much more extensive than previously thought and appear to be important in emotional learning. Edited by Plum F. BEI. The actual mechanism of LTP in the amygdala is not as important as the fact that we can now ask questions about the mechanisms of synaptic plasticity in a structure with such a clear role in a well characterized learning and memory phenomenon. 1972: 131-162. An excellent review of research on the role of the human amygdala in emotion. Washinton DC: American Physiological Society. 1992. In Emolions: Neu- DG: Memory: Anatomical Organization of Candidate Regions. 2: 1395%1420. . in broad outline. Behavior. 1981:77-90. Edited by I lill D.amygdala in behavioral tasks used to study emotion in experimental animals. by LJS Public lkalth Service Grants MH38774 and of emotion and emotional learning ral and Chemical Control. BUCY P: “Psychic BIindnesSj’.. Am J Pbysiol 1937. 16. Panksepp J. KNAPP M: Organization of rhe Amygdalopetal Projections from Modality-Specific Cortical Association Areas in the Monkey. Memoq: and Mental Neurohiological Aspccl. 13. I: i%e Ner L~OUSSystem. Keseurcb and Ez@erience Edited by Plutchil R. which is difficult to define. FONRERGE: Control of Emotional Behavior Through the Hypothalamus and AmygdaIoid Complex. 1982. In Emotion: Tbeoly. 1: Neuropb siology Edited by Field J. A critical discussion of the limbic system concept as it relates to emotion. This is one of the few 195 . in press. 1987. In Handbook of P@siolog)~. 14. 191:515-543.a@. Edited by Oomur Scientific Societies Press. have been highlighted as: of special interest of outstanding interest reading within the annual period of re- GLOOR P: Amygdala. Higher Furzctions of the Bruin. LEDorrx JE: Emotion and the LImbic System Concept. “- 9. A comprehensive collection of chapters on the structure and function of the amygdala. New York: Wileytiss. 12. These discrepancies need to be ac -. Bethesda: American Physiological Society. The paper concludes that the so-called limbic system. FARD CR: Neurons of the Acoustic Thalamus that Project to the Amygdala Contain Glutamate. Magoun 11. Memov and Mental Dys juzction. In Handhook of P@Yo@y. SIE(.x. 49:381-391. MISI~KINM: The AmygdaIa: Sensory Gateway to the Emotions. Bethesda: American Physiological Society. Edited by Morgane PJ. cepts Neurosci 1991. 1. as expressed behaviorally. VAN HCXWN GW: The Differential Distribution. New York: Marcell Dekker. Amsterdam: ElseviedNorth Holland Biomedical Press. WEIXR~NTZ L: Behavioral Changes Associated with Ablation of the Amygdaloid Complex in Monkeys. Higher Fzuzctions of the Umin. References and recommended Papers of particular interest. 5:41’+460 19. of the AmygdaIa In 7hc Am_ygdala: Neurobiological A. Brain 15. 8. The Nervous $stem. Beballioral Study ies of the H@othalamtu. This paper demonstrates the presence of glutamate in cells of origin of the auditory thakimwamygdala projection. 5:407467. published view. 2~169-199. 11. there are many possible reasons why this may be so. 3:203-240. That this phenomenon plays such a central role in normal mental life makes this an especially attractive system for future investigation. TIXNER BH. This review shows that the amygdala has been implicated in essentially every such task. Edited by BenAri Y.. Orlando: Academic Press.. has little to do with emotion and that the survival of the limbic system hypothesis of emotion is in large part due to the fact that the amygdala is part of this system. PANKS~PPJ: Toward a General Psychobiological Emotions. 134:145-149. In recent years. in press.

1991:229-254 This chapter reviews recent work by Kapp’s lahoratoty on the contribution of the central nucleus of the amygdala to cortical arousal processes. 5:137-167. In Handbook ofPbysiolo~. . WHAIRN PJ. In 7br At?!)r&kz~: Neur(hiohgical hpccts ofEmo tion. 22:230-246. of Emotion. Shows that projections to the amygdala from thalamic and cortical areas of the auditot). Ctcc~~e’rri P. PI’I’KANEN A.Memq~ and Mcwtal Dy@nctiort. 5:29>371. . Neuroscience 1991. GIUIIAM PW. 20. 1:207-220. Suggests the possibility that the amygdala may play an imporrant role in the integration of sensory signals of vatying degrees of complexity in the initiation and control of emotional reactions. . III’KHCOCK JM. Bethesda: Americdn Physiological Society.&Y . is the suggestion that receptive field piasticity depends upon cholinergic transmission to the cortex from the amygdala by wdy of the nucleus hasalis. FAKI~CR. pioneered In previous work by Holland. Edited by Bower GH. . Of special significance is the presentation of findings showing that stimulation of the central nucleus of the amygdala produces cortical arousal (electroencephalogram desynchronizdtion) and that this effect is blocked by systemic administration of the cholinergic antagonist att-opine. L&l) Ihzin Km 1991.ty LEIXNJXJE. Areas of the Thalamus and Cortex. ME’I’HEKATE R. 1987. 29.. 1: T%e Nertjous System. This is an excellent study showing for the first time that subtotal lesions of the primate amygdala could produce the emotional changes of the Kli_iver-Bucy syndrome and at the same time not produce the cognitive memory deficits. HOIIANDPC: The Amygdala Central Nucleus and Appetitive Pavlovian Conditioning: Lesions Impair One Class of Conditioned Behavior. Fear and Kuge. DIAMOND D. 313:295-325. Crccr~r. WHITE EL: The Lateral Nucleus of the Amygdala Mediates Expression of the Amphetamine Conditioned Place Preference. 27. This study. TURNERBH. Bruin Kes 19X4. 1987. Higher Functions of the Bruin. New York: Guildford. . AMA&U DG: Demonstration of Projections from the Lateral Nucleus to the Basal Nucleus of the Amygdala: a PH. 5:25-83. IIIKOI NM. SAWCIIENKOPE: Anterograde Neuroanatomical Tracing Method that Shows the Detailed Morphology of Neurons. Of particular relevance. MCKENNAT. In 7& Pvc/&om oJ’Learning and I%fotit~ation.‘rr‘i P. I~\YXINS RD. MassachusettS: MIT Press. IWATAJ. The study also shows that the central nucleus of the amygdala contributes to appetitive conditioning. CANNON WF: Bodi!y Cbunges in Pain. Edited hy Plum F.. 79~217-224. which projects widely to cortex. S~II’PL~~ WF. .. 1929. This study identifies a previously unknown projection from the lateral to the basolateral nucleus of the amygdala and clarifies how sensor) inputs tllat reach the lateral nucleus get distributed to other amygclaloid regions and to cortical association areas. SQUIRE LR. 39. Bethesda: American Physiological Society. S. 21. Square LR. 1 I:2107~2116. 38. The ohsetvation that the amygdala receives extensive sensory inputs from thalamic areas will force further considerations of the pas sthle contribution of thalamcramygdala projections to hehaViOrdl func~ tions. fZz@ Rrain Rcs 1991. Phaseolus Leucoagglutinin.I Neurosci 1990. 1987.&MORG. In Hundbook of Physiology I: The Nenwls gcrtem. ~HE J. O’BKIEN A. XA~URARISA. 23. KVV BS. is used to teaye apart the contribution of the central nucleus of the amyg dala to conditioned responses r&ted to a conditioned stimulus versus an apprtttwe unconditioned stimulus. ROM. CII\KK GA. A novel behavioral analysis.. ROH~INS TW The Basolateral AmygdaIa-Ventral Striatal System and Conditioned Place Preference: Further Evidence of Limbic-Striatal Interactions Underlying Reward-Related Processes. Hippocampus 1991. L~Dor’x jections tonomic Nrurosci JE.&L Study in the Monkey. This study together with that of Hiroi and White [33*-j shows that the lateral amygdaloid nucleus is an essential component of appetitive as well as aversive emo~ tional learning circuits. In Ham&wok oj’Physiology.ER MA: The AmygdaIa: a Neuroanatomical Systems Approach to its Contributions to Aversive Conditioning. which appear to he more related to the hippocampai fommation. San Diego: Academic Press. and that this system. LENNARZKTZ R. 105:19061911. . New York: Wiley Liss.. GERFEN CR. Elunger. BARD P: The Central Representation of the Sympathetic System: as Indicated by Certain Physiological Observations. 24. This is the first electron microscopic study of a&rent projections to the amygdala. 22.. Pkscot: JP: AmygdaIoid Contributions to Conditioned Arousal and Sensory Information Processing.. .4NSKIL: Overlapping Projections to the AmygdaIa and Striatum from Auditory Processing Neurosci Lett 1991. ZOL. P. New York: Appleton. 25./ Nccurosci 1990. Edited by Gabriel M. E\‘FNTT BJ. 10:1062~1069. In Leurning and Computational Neuroscience: Fowzah fions of Adaptive Netulorks. MOKIUSKA. ROSEN JB: Anxiety and the Amygdala: Pharmacological and Anatomical Analysis of the FearPotentiated Startle Paradigm. ROMANSKILM: The Lateral Amygdaloid Nucleus: Sensory Interface of the AmygdaIa in Fear Conditioning. 83:465-470. . 37. .!$ 8:2517-2529. 34. system overlap. especially in light of the findings by Kapp and associates (see [36**] ). Moore J. their Axons and Terminals: Immunohistochemical Localization of Axonally Transported Plant Lectin. 36. SQCIIKFLR: Memory: Neural Organization and Behavior. REIS DJ: Different Proof the Central Amygdaloid Nucleus Mediate Auand Behavioral Correlates of Conditioned Fear. ECCIESJC: Mechanisms of Learning in Complex Neural Systems. KANDELER: Cell Biological Studies of Learning in Simple Vertebrate and Invertebrate Systems.I 198. Edited by Plum F. P&<:oE JP.FH N. PAI)EZJW: A Proposed Mechanism Pychiatr 1937. FARB CR. Higher Functions of‘the Brain. BIXI. Cambridge. It shows that the projections make asymmetric (excitatory) synaptic con@&. 1987..196 Cognitive neuroscience instances where a possible transmitter projections to the amygdala.. tom gether wtth that of Eve&t and colleagues [34**] shows that the lateral amygcidloid nucleus is an essential component of appetitive as well as aversive emotional learning circuits.gxhiatr 1929. Arch Neural P. 35. CLOWER RP: Independence of Memory Functions and Emotional Behavior: Separate Contributions of the Hippocampal Formation and the AmygdaIa. 1s responsible for the cholinergicallymediated arousal effects. Bethesda: American Physiological Society. 31 32. 1: The Nert~ous System Higher Functions oJ the Bruin. 28. MILWR TA: Ultrastructure and Synaptic Associations of Auditory Thakimo-AmygdaIa Projections in the Rat. The authors propose that central nucleus stimulation activates the cholinergic neurons of the nucleus basatis. WEINI~EK~. 42:1-l& Prevtous studies had implicated the lateral nucleus as the sensory interface of the amygdala in fear conditioning (see [ 281). LEIX~I’XJE. . . 1984. Ckss~u. 85:577-586. 40. 134:139-144. In Newopsycholo$y of Memory Edited b) Buttl?r N. J Nrurosci 1991. . 50 i>Avth M. GALLAGHER M.I Camp Neural 1991. . 26.. A survey of thalamic projections to the amygdala and an extensive scholarly review of the implications of thalamic sensory afferentation of this structure. BAKINGJ. Edited by Plum F. Edited by Aggleton J. has been identilied in sensc. .u J: Neural Adaptive Information Processing: a Preliminary Model of Receptive-Field Plasticity in Auditory Cortex During Pavlovian Conditioning. which is consistent with the observations that the cells of origin of the projection contain glutamate (see [ 19**] 1. Previous studies had implicated the lateral nucleus as the sensory ins t&ace of the amygdala in fear conditioning (see [28] ). This chapter reviews the work of Wemherger’s lahoratoty on recepnve field plasticity in auditoty cortex during aversive classical conditioning. HEKKENHAMM: Thalamoamygdaloid Projections in the Rat: a Test of the AmygdaIa’s Role in Sensory Processing. 33. KAPP BS. 290:21F238. 1990:91-138. Arch Neural LED0l!X JE.

MONAGHAN DT. the two studies would support each other in implicating NMDA receptors in fear conditioning. . 43. JE LeDoux.Brain mechanisms 41. BROWN TH: Long1990. 45.:Induction of Long-Term Potentiation in the Basolateral Amygdala does not Depend on NMDA Receptor Activation. and emotional learning LeDoux LANDER&FERNANDEZ J. however.phosphonopentanoate (Al%‘) and is thus ambiguous as to where the action occurs. Annu Rezl 1987. MISERENDINO MJD. of emotion KIM JJ. 345:71&718. KEENAN CL: Long-Term Synaptic Potentiation. Of. MONAGHANDT. Center for Neural Science. 49. one can speculate that the effects occur in the amygdala. [47**].raemory processes. FANXELOW MS: N- Methyl-D-Aspartate Receptor Antagonist APV Blocks Acquisition but not Expression of Fear Conditioning. DECOLA JP. Nature 1990. Term Synaptic Potentiation in the Amygdala.. This study shows that NMDA receptors in or near the amygdala play an essential role in emotional learning. Synapse 1992.?? and in relating synaptic plasticity to normal. BELLAVANCE LL. Science 1988.. CHAPMANPF. 11:61-80. 47. BROWN TH.. the mechanism. 44. . Annu Recj Neurosci 1988. and the findings only show that this form is independent of NMDA receptors. Together with the study by Miserendion et a(. COTMAN CW: Distribution of N-Methyl-DAspartate-Sensitive L-(3H)Glutamate-Binding Sites in Rat Brain. 197 . however. CHAPMAN PF. . It is still possible Fiat an NMDA~ dependent form of LTP will be found. GANONG AH: Excitatory Amino Acid Neurotransmission: NMDA Receptors and Hebb-Type Synaptic Plasticity.~ynapse 6:271-278. 46. This study involves i. TEYLERTJ.46] 1. This study is potentially damaging to the hypothesis that synaptic plas ticity in the amygdala underlies emotional learning. New York 10003. and that both synaptic plasticity and emotional learning depend upon NMDA receptors (see [47**] ). 242:724-728. 105:16&167. Regardless.ltraventricular injection of 2~amino-5. CHAPMANPF. This is not the only form of LTP that has been demonstrated in the amygdala. . SANANESCB. LEDOL~X JE: Synaptic Plasticity in Fear Condi- tioning Circuits: Induction of LTP in the Lateral Nucleus of the Amygdala by Stimulation of the Medial Geniculate Body. 10:281%2824. New York University. 48. New York. CLUCNETMC. USA. 6 Washington Place. COTMAN CW. This fits well with the growing evidence of synaptic plasticity in the amygdala (see [45. KAKGS EW. MEUA KR. DAVIS M: Blocking of Acquisition but not Expression of Conditioned Fear-POtentiated Startle by NMDA Antagonists in the Amygdala. 42. KAIRISS EW. KENNAN CL. amygdala LTP is a new and exciting research a& th% bffefs new posof 'e&&onal memory sibilities in understanding cellular mechanis. J Neurosci 1986. Behall Neurosci 1991. in press. 10:131&161. If so. 5:290+2919. DISCENNAP: Long-Term Neurosci Potentiation. J Neurosci 1990.