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rain mechanisms of emotion and emotional learning
J oseph
E
LeDoux
New York
University, New York, New York, USA
The amygdala appears to play an essential role in many aspects of
emotional information processing and behavior. Studies over the past year
have begun to clarify the anatomical organization of the ainygdala and the
contribution of its individual subregions to emotional functions, especially
emotional learning and memory. Researchers can now point to plausible
circuits involved in the transmission of sensory inputs into the amygdala
between amygdaloid subregions and to efferent targets in cortical and
subcortical regions, for specific emotional learning and mem ory processes.
Current Opinion in Neurobiology 1992, 2:191-197
Introduction
Research
over the past 40 years has pointed to the amyg-
dala as the heart and soul of the brain’s emotional net-
work [l-5,6=*,7**]. Following Kluver and Bucy’s [8] oh-
servation 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 exper-
imental task that has been used to study emotional rep-
resentation in the brain. No other brain a rea 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 com ponent 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 amyg-
dala to emotional processes.
In spite of the clear involvement of the amygdala in emo-
tional functions, until recently little progre ss had been
mad e in understanding the functional organization of the
amygdala in emotion. In the older anatomical literature
the amygdala w as 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 th at
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 subarea s to
different aspects of emotional functions. The emphasis of
this review will therefore be on recent advances in our
understanding of the anatom ical organization of individ-
ual amygdaloid subareas and the role of these subareas
-,
-;. -
I.
.I
.:
’ L,
A
in emotiona l functions, esp ecially emotional learning and
memory.
Anatomical organization of the amygdala
The emotional functions of the amygdala critically de-
pend upon the reception of sensory inputs. Many of
the sensory projections to the amygdala terminate in
the lateral amygdaloid nucleus. These projections origi-
nate mainly in the sensory processing areas of the cor-
tex and thalamus. W hile the cortico-amygdala projec-
tions had been well characterized at the light micro-
scopic 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
thalam us originates primarily in the posteri or intralami-
nar 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, sug-
gesting that neural transmission in this pathway may be
mediated by this excitatory amino acid transmitter sub-
stance [19 ]. Furthermore, the synaptic profile of these
terminals [20**] is similar to that of glutamate-containing
terminals in this region (CR Farb and JE LeDoux, unpub-
lished 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 thalamwamygd ala projections across sensory modal-
ities has been carried out by Turner and Herkenham
[21 ]. Radiolabeled amino acids were injected into var-
ious thalamic nuclei and transport to the amygdala was
Abbreviations
LTP-long-term potentiation; NMDA-N-methyl-o-aspartic acid; Pha-L-fhaseolus vulgaris leucoagglutinin
@ Current Biology Ltd ISSN 0959 4388
191
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192 Cognitive neurosc ience
Arousal and plasticity
Lemniscal
auditory
pathways
Extralemniscal
auditory
pathways
Behavioral Autonomic Endocrine
Emotional response control systems
Fig. 1. A diagram illustrating some of the pa thways underlying emotional informatton processing and response control by the amygdala.
Pathways through whic h auditory inputs a re transmitted to the amygda la are shown but similar circuits a lso exist for other sensory
systems. Tonotopica lly organized auditory signals are transmitted to the auditory thalamus over lemnisca l pathways, which synapse
in the ventral d ivision of the medial geniculate body (M I. Extralemniscal pa thways transmit to other parts of the auditory thalamus,
including the medial division of the media l geniculate body (MC m) and the posterior intralaminar nucleus (PIN). While MG v only projects
to primary a uditory cortex, MCmiPlN projects to both primary and assoc iation areas of auditory cortex, as well as to the lateral nucleus
of the amygdala (AL). The thalamo-amygda la projection forms asymmetric, excitatory (+ 1contacts with AL, contains glutamate (C lu),
and may use this excitatory substance as a neurotransmitter. Thalamo-amygda la projections have been implicated in emotional learning,
and high-frequency stimulation of these projections produces long-term potentiation (LTP) in AL. Auditory and polymodal assoc iation
areas relay auditory signals to AL by way of the external ca psule. These pathways are also involved in emotional learning and exhibit
LTP. AL projects to the basolateral nucleus of the amygdala (ABL), which projects wide ly to corttcal a reas (not shown) and to the central
nucleus of the amygdala (A CE). ACE has extensive connec tivity with brainstem areas involved in the control of emotional responses. It also
projects to the nucleus basalis, which projects wide ly to co rtica l areas. The pathway from the nucleus basalis to cortex uses ac etylcholine
(AC h) as a neurotransmitter. Cholinergic transmission to the cortex from the nucleus ba salis has been implica ted in co rtica l arousal a nd
plasticity.
examined. Their findings show that the amygdala receives
subcortical inputs from a wide variety of sensory systems.
emotional situations. Direct projections to the amygdala
have not figured prominently in contemporary thought
about the neural basis of emotion, which tends to focus
ThalamWam ygdala projections have been implicated in
on corticcramygdala systems [l-5,7-,13-]. The classic
emotiona l learning processes , especially fear condition-
theories of Cannon [22], Bard [23] and Papez [24],
ing (see [6**] ). Thalamic inputs to the amygdala allow
however, emphasized the importance of subcortical sen
sensory signals to activate it either before or simulta
sot-y transmission in the experience and expression of
neous with the arrival of signals at the cortical level,
emotion. These theories suggested that the hypothala-
and may therefore play an important role in precon-
mus, when activated directly by sensory projections from
scious and precognitive emotional processing. Because
the ventral thalamus, gave rise to emotional behavior
these projections exit the primary sensory systems at
by way of projections to the brainstem and gave rise
an early stage of processin g, they are unlikely to en-
to subjective emotional experiences by way of projec-
code complex stimulus representations. They may allow
tions to the cerebral cortex. The finding of extensive
primitive sensory representations to rapidly activate the
subcortical sensory innervation of the amygdala by thala-
amygdala, however, which may be important in certain
mic projections fits well with the spirit of these theories,
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Brain mec hanisms of emotion and emotional learning LeDoux
193
even if the anatomical details (thalamo-amygdala versus
thalamo-hypothalamic projections) are different.
Our knowledge of anatomical interactions between
thalamwamygd ala and corticcl-amygdala connections is
in its infancy, but prog ress in this area is essential for
understanding how the amygdala integrates diverse sen-
sory inputs in emotiona l information processin g. Within a
given sensory m odality, the two projection systems over-
lap and may in fact converg e in the lateral nucleus [25-l,
Convergence would allow thalamic and cortical sensory
inputs to act on common ensembles of amygdala neu-
rons, and would place the lateral nucleus of the amyg-
dala in a key position to coordinate the flow of sensory
information that ultimately leads to emotional reactions.
Given that much o f the sensory ctierentation of the amyg-
dala is by way of the lateral nucleus, connections from
this nucleus to other amygdaloid regions must play an
important role in the emotional processing functions of
the amygdala. Until recently it had been technically cum-
bersome to study the intrinsic organization of the amyg-
d&. The problem is that its subregions occupy small
volumes and therefore it is diffkult to restrict the injec-
tion of tracer substances to one region. T he introduc-
tion of the Pbaseolus vulgaris leucoagglutinin (Pha-L)
axonal transport neural tract-tracing method [261, which
allows for the placement of very restricted injection sites,
identification of cells involved in uptak e and transport,
visualization of full axonal arboriza tions, and identifica-
tion of synaptic boutons at the light microscopic level,
has solved this problem and has provided some new
insights into amyg dala organization. Pittinen and Am aral
[27**] placed injections of Pha-L into the lateral nucleus
and demonstrated a previously unknown projection to
the basolateral nucleus in primates. Studies in rats have
confirmed the existence of this projection (JE Ledoux,
CR Farb, L Steffanacci, G Go, A Pitkanen and DG Amaral,
unpublished data). These observations are of significance
for several reasons . First, unlike the lateral nucleus, the
basolateral nucleus projects heavily to cortical association
areas [14,27-l. Sensory information reaching the lateral
nucleus from either cortex or thalamus can thus influence
on-going cortical processing by way of the lateral to ba-
solateral projections. Secon d, unlike the lateral nucleus,
the basolateral nucleus projects heavily to the central nu-
cleus of the amygdala [14,151, which, as described below,
provides a link by which sensor)i inputs to the lateral
nucleus can activate emotional behaviors and autonomic
response s, and can influence cortical arousa l.
Functional spec ialization within the amygdala
As described above, most of the sensoty projections to
the amygdala terminate in the lateral amygdaloid nucleus.
It might be expected that lesions of this structure would
disconnect the amygdala from environmental informa-
tion and therefore reproduce the disruptive effects on
emotional functions of both large amyg daloid lesions, in-
volving several subregions (including the lateral nucleus),
and small lesions o f other subregions of the amygdala.
Recent studies have in fact shown that lesions confined to
the lateral nucleus prod uce the predicted ‘disconnection’
effects in several different behavioral tasks. One study of
rodents involved classica l fear conditioning, a proce dure
whereby an affectively neutral stimulus, such as a tone,
is paired with a footshock [281. After several pairings
the tone elicits emotional (fear) reactions, such as ‘freez-
ing’ and changes in autonomic activity. A large sample
size was necessary to generate a small group with ac-
ceptable lesions, i.e. lesions that completely destroyed
the lateral nucleus at a designated level of the amygdala,
and that did not encroach upon the central nucleus of
the amygdala, a structure that is known to be necessary
as an amygdaloid output in the expression of emotional
respons es [2 +3l]. Similarly, studies of non-human pri-
mates have shown that subtotal lesions of the amygdala
that encroach upon th e lateral nucleus produce the loss
of fear and other components of the Kliiver-Rucy syn-
drome [32*-l.
The lateral nucleus has also been it?ipli&@ .in appet-
itive emotional reactions, particula@ .conditioned place
preference learning in rodents [33**,34*0]. Conditioned
place preferences are established by providing reinforc-
ing stimulation in a certain location. This can be done
with either primary reinforcers (such as desirable foods)
or by chemical or electrical brain stimulation. Lesions of
the lateral/basolateral amygdala interfere with the forma-
tion of these conditioned place preferences. 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, where sensory information
may normally be associated with reward information by
interactions with dopam ine containing terminals.
Thus, the lateral nucleus of the amygdala, by virtue of
its input from sensory processing structures, appears to
be involved in both place preference formation and fear
conditioning, but seems to use different e&rent projec-
tions in these forms of learning; place preferences appear
to involve projections to the nucleus accumbens and fear
conditioning involves projection s to the central nucleus
of the amygdala.
The central nucleus of the amygdala is not exclusively
involved in aversive emotiona l learning. Recen t studies by
Gallagher, Graham and Holland [35**] show that it is also
involved in appetitiv e conditioning. IJsing a task whic h
separates out conditioned responses related to the con-
ditioned stimulus, and those related to the unconditioned
stimulus, they found th at central nucleus lesions selec -
tively impaired conditioned-stimulus related responses.
This kind of behavio ral analysis has not yet been per-
formed for other conditioning paradigms.
The central nucleus of the amygdala, by way of its ex-
tensive connectivity with brainstem areas, is believed
to play an important role in the expression of behav-
ioral and autonomic responses associated with emotional
arousal. This notion was first demonstrated in studies of
conditioned bradycardia by Kapp and coworkers [29],
and later extended to several other response modalities
[30,31]. 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 neocor-
tex. Thus, electrical stimulation of the central nucleus
produces cortical electroencephalogram desynchroniza-
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194 Cognitive neurosc ience
tion. As this effect is abolished by systemic administra-
tion of the cholinergic antagonist atropine, it is believed
that connections from the central nucleus to the cholin-
ergic neurons of the nucleus basalis, which projects
widely to the neocortex, mediate these changes. This
cholinergic arousal system may allow emotional infor-
mation processing by the amygdala (particularly by the
lateral-baso later&c entral connection) to influence per-
ceptual, attentional, memory, and other cognitive pro-
cesses mediated at the neocortical level.
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 receptiv e field functions of neurons in auditory cortex
critically involve parallel transmission and convergen ce of
two pathways: pathway one, a specific (lemniscal) relay
of tonotopic auditory information from the ventral divi-
sion of the medial geniculate body to the auditory cortex;
and pathway 2, an extralemniscal relay from the medial
areas of the medial geniculate body to the amygdala,
which then projects to the nucleus basalis, which p rojects
widely to cortex. Weinberger proposes that pathway 2
enters into ‘Hebbian synapses’ with pathway 1 and as
a result modifies the receptive fields of the involved
neurons. More specifically, the thalamo-amygdala pro-
jection to the nucleus basalis increases the postsynaptic
excitability of pyram idal cells in auditory cortex (cells
that receive the frequency-specific inputs from the ven-
tral division of the medial geniculate body), and thereby
changes the strength of inputs of that frequency. Thus,
thalam cl-amyg dala transmission is not only essential for
subcortical emotional learning and non-specific arousal
(see above), but may also contribute to highly specific
plastic modifications occurring in the cerebral cortex.
Cellular mec hanisms of emotional learning in
the amygdala
It is widely believed that synaptic plasticity underlies
the rapid induction of memories through experience
(see [3%40 ]). One of the most extensively studied
models of synaptic plasticity is long-term potentiation
(LTP) [41-43], which involves an increase in the eff-
cacy of synaptic transmission as a result of high fre-
quency (tetanizing) stimulation of an afferent pathway.
In some hippocam pal pathways, LTP is mediated by ex-
citatory amino acid receptors [41-43]. It is thus signifi-
cant that the excitatory amino acid, glutamate, is present
in the cells of origin of at least some sensory inputs
to the lateral nucleus of the amygdala [ 19**], and that
excitatory amino acid receptors are highly concentrated
in the lateral/basolateral region [44]. Further, LTP has
been induced in the lateral/basolateral amygdala by stim-
ulating thalameamygdala projections n zt zlo 45], and
corticwamygdala projections (the external capsule) in
v tro [46]. Lesions of the lateral nucleus interfere with
fear conditioning [28] and blockade of N-methyl-D-as-
pat-tic acid (NMDA ) receptors in the lateral/basolateral
amygdala interferes with the acquisition [47**] of fear
conditioning. It has also been show n that intraventric-
ular injections of NM DA antagonists interfere with the
acquisition but not the expressio n of fear conditioning,
presumably by acting in the amygdala [48-l.
Collectively, these findings suaest that excitatory amino
acid receptors in the amygdala may play a rU id role
in synaptic transmission and synaptic plasticity in the
sensory projections to the amygdala, and in emotional
learning processing mediated through th ese projections.
A recent
n v tro
study of LTP, however, suggests that
synaptic plasticity in the amygdala is not mediated by
NM DA receptors [49**]. Because of the important im-
plications of this finding, it needs to be considere d in
some detail. Several points should be noted. First, the
study involved stimulation of the external capsule, w hich
contains fibers from many areas o f the neocortex. It is not
known whether all or only some of the projections trav-
eling through the external capsule are plastic. Selective
tetanization of the individual cortical areas that project to
the amygdala would be useful. Second, given the diverse
origins of the fibers stimulated, it is possible that NMD A
and non-NMDA (and possibly even non-excitatory amino
acid) mechanisms are involved in the overall effect. In the
hippocampus, LTP in some p athways is NMD A depen-
dent while in others it is not. If multiple mechanisms are
involved in external capsule LTP, blockade of only the
NM DA receptors would not completely block LTP. Fu-
ture studies should determine which substances are used
in normal transmission and synaptic plasticity by projec-
tions from individual cortical areas. Third, the recordings
were m ade in the lateral and basolateral nuclei. The cor-
tical inputs to the lateral and basolateral nuclei a re very
different. The lateral nucleus receives m uch of the direct
sensory innervation from cortex and thalamus and then
projects to the basolateral nucleus, which also receives
tierents from non-sensory association regions. Careful
comparisons therefore need to be made between synap-
tic plasticity in the lateral versus basolateral areas. Fourth,
even if corticcramygdala LTP turns out not to involve
NM DA receptors, the case would still be open with re-
spect to thalamo-amygdala projections. Thus, although
the observation that blockade of NM DA receptors in the
lateral/basolateral amygddki fails to interfere with LTP is
one of the most important findings of the past year, its
implications for understanding synaptic plasticity in the
amygdala should not be over interpreted at this point.
This area of work has just begun and much more work
needs to be done.
Regardless of the mechanism, amygdala LTP is extremely
important. It is induced in pathways that are known to
have clear roles in well characterized and specific learning
processes. Like LTP, the conditioned associations medi-
ated by the amygdala are rapidly learned and long last-
ing. Furthermore, 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.
This close correspondence between LTP and behavior
has been lacking for the hippocampus and has hindered
progress in relating hippocampal LTP to real-life learn-
ing and memory phenomena. Although the amygdh will
always lack the convenient anatomical organization of
the hippocampus, studies of amygdala LTP may help to
uncover basic mechanisms through which normal and
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Brain mechanisms of emotion and emotional learning LeDoux 195
pathological emotional memories are formed, and may
also be useful as a model system for furthering our un-
derstanding of the relationship between LTP and mem-
ory.
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apan
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6.
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LEDOUX JE: Emotion and the AmygdaIa. In The Am.y&zla:
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Edited by Aggleton J. New York: Wileytiss; 1992, in
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Conclusions
The amygdala has long been view ed as playing an impor-
tant role in emotion. In recent years, however, there h as
been an explosion of research aimed at understanding
the anatomical organization of this structure and its con-
tribution to emotion . New findings relating to the organi-
zation, especially those concerned with how sensory in-
puts reach and are subsequently distributed throughout
the amygdala, have been especially helpful, as they begin
to provid e, in broad outline, an anatomi cal understanding
of the input-output relations t hat underlie information
processing by this structure. 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, as expressed behav-
iorally, and may also contribute to cortical arousal and
plasticity in emotional situations. Although blockade of
NM DA receptors in the amygdala does not interfere with
LTP, there a re many possible reasons why this may be
so, and it is too early to conclude that the amygdala does
not have an NMD A-mediated form of LTP. 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 mem ory
phenomenon. That this phenomenon plays such a cen-
tral role in normal mental life mak es this an especially
attractiv e system fo r future inve stigation.
A thorough review of the involvement of the ,amygdala in behavioral
tasks used to study emotion in experimental animals. This review shows
that the amygdala has been implicated in essentially every such task.
7.
. .
HALGRFN E: Emotional Neurophysiology of the AmygdaIa
within the Context of Human Cognition. In 7hc
Am_ygdala:
Neurobiological A.spects of Emotion, Memory. and Mental 0~1s~
function. Edited by Aggleton J. New York: WileyLiss; 1992, in
press.
An excellent review of research on the role of the human amygdala in
emotion. The review points out certain discrepancies between findings
from human and animal research. These discrepancies need to be ac
counted for.
-,
8. KI.~NER H, BUCY P: “Psychic BIindnesSj’.,a@,Other Symp-
toms Following Bilateral TemporalZol&tom+ in Rhesus
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Am J Pbysiol 1937,
119;2?2;353. “-
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WEIXR~NTZ L: Behavioral Changes Associated with Ablation
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~sychol 1956, 49:381-391.
10.
LEDorrx JE: Emotion and the LImbic System Concept. Con-
. .
cepts
Neurosci 1991, 2~169-199.
A critical discussion of the limbic system concept as it relates to emo-
tion. The paper concludes that the so-called limbic system, which is
difficult to define, 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.
11.
PANKS~PP : Toward a General Psychobiological Theory of
Emotions.
Beball Brain Sci
1982, 5:407467.
12. SIE ;ELA, EIXNGER H: Neural Control of Aggression and Rage
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f~andbook of the tf@othalamus,
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cknowledgement
13.
AGGLE’I’ON: The
Am&ala- Neurohiological Aspccl.s of Emu
. . tion, Memoq: and Mental Dysjunction. New York: Wiley-L&;
1992, in press.
Supported by LJS Public lkalth Service Grants MH38774 and
MH465IG.
,
A comprehensive collection of chapters on the structure and function
of the amygdala. It is the most thorough survey of the amygdala available
toddy.
14.
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Areas of the Thalamus and Cortex. Neurosci Lett 1991,
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Shows that projections to the amygdala from thalamic and cortical areas
of the auditot), system overlap. Suggests the possibility that the amyg-
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vatying degrees of complexity in the initiation and control of emotional
reactions.
26.
GERFEN CR, SAWCIIENKO PE: Anterograde Neuroanatomical
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to the basolateral nucleus of the amygdala and clarifies how sensor)
inputs tllat reach the lateral nucleus get distributed to other amygclaloid
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the AmygdaIa. Hippocampus 1991, 1:207-220.
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, which appear to he more related to the hippocampai
fommation.
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IIIKOI NM, WHITE EL: The Lateral Nucleus of the Amyg-
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t&ace of the amygdala in fear conditioning (see [28] ). This study, 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.
34.
E\‘FNTT BJ, MOKIUSKA, O’BKIEN A, ROH~INS TW The Baso-
. .
lateral AmygdaIa-Ventral Striatal System and Conditioned
Place Preference: Further Evidence of Limbic-Striatal Inter-
actions Underlying Reward-Related Processes. Neuroscience
1991, 42:1-l&
Prevtous studies had implicated the lateral nucleus as the sensory inter-
face of the amygdala in fear conditioning (see [281). 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.
35.
GALLAGHER M, GIUIIAM PW, HOIIAND C: The Amygdala Cen-
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tral Nucleus and Appetitive Pavlovian Conditioning: Lesions
Impair One Class of Conditioned Behavior. ,I
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105:19061911.
A novel behavioral analysis, pioneered In previous work by Holland, 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, The study also shows that the
central nucleus of the amygdala contributes to appetitive conditioning.
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KAPP
BS,
WHAIRN
PJ, S~II’PL~~F, Pkscot: JP: AmygdaIoid Con-
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This chapter reviews recent work by Kapp’s lahoratoty on the contri-
bution of the central nucleus of the amygdala to cortical arousal pro-
cesses. 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 at-
t-opine. The authors propose that central nucleus stimulation activates
the cholinergic neurons of the nucleus basatis, and that this system,
which projects widely to cortex, 1s responsible for the cholinergically-
mediated arousal effects.
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WEINI~EK~;FH , ~HE J, ME’I’HEKATE , MCKENNA T, DIAMOND
. . D, BAKINGJ, LENNARZKTZ, Ckss~u,u
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ing. In Leurning and Computational Neuroscience: Fowzah
fions of Adaptive Netulorks. Edited by Gabriel M , Moore J.
Cambridge, MassachusettS: MIT Press; 1990:91-138.
This chapter reviews the work of Wemherger’s lahoratoty on recepnve
field plasticity in auditoty cortex during aversive classical conditioning.
Of particular relevance, especially in light of the findings by Kapp and
associates (see [36**] ), is the suggestion that receptive field piasticity
depends upon cholinergic transmission to the cortex from the amyg-
dala by wdy of the nucleus hasalis.
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tions oJ the Bruin. Edited by Plum F. Bethesda: Americdn
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I~\YXINS RD, CII\KK GA, KANDELER: Cell Biological Studies
of Learning
in Simple Vertebrate and Invertebrate Systems.
In Ham&wok oj’ Physiology, 1: T e Nertjous System. Higher
Functions of‘the Brain. Edited hy Plum F. Bethesda: American
Physiological Society; 1987, 5:25-83.
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ECCIESJC: Mechanisms of Learning in Complex Neural Sys-
tems. In
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BROWN TH, CHAPMANPF, KAKGS EW, KEENAN CL: Long-Term
Synaptic Potentiation. Science
1988, 242:724-728.
TEYLER J, DISCENNA : Long-Term Potentiation.
Annu Rezl
Neurosci 1987, 10:131&161.
COTMANCW, MONAGHANDT, GANONG AH xcitatory Amino
Acid Neurotransmission: N MDA Receptors and Hebb-Type
Synaptic Plasticity. Annu Recj Neurosci 1988, 11:61-80.
MONAGHANDT, COTMAN CW:
Distribution of N-Methyl-D-
Aspartate-Sensitive L-(3H)Glutamate-Binding Sites in Rat
Brain.
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CLUCNETMC, LEDOL~XE: Synaptic Plasticity in Fear Condi-
tioning Circuits: Induction of LTP in the Lateral Nucleus
of the Am ygdala by Stimulation of the Medial Geniculate
Body.
J Neurosci 1990, 10:281%2824.
CHAPMAN PF, KAIRISS EW, KENNAN CL, BROWN TH: Long-
Term Synaptic Potentiation in the Amygdala. .~ynapse990,
6:271-278.
MISERENDINOJD, SANANES B, MEUA KR, DAVIS M: Blocking
of Acquisition but not Expression of Conditioned Fear-PO-
tentiated Startle by NMDA Antagonists in the Amygdala.
Nature 1990, 345:71&718.
This study shows that NMDA receptors in or near the amygdala play
an essential role in emotional learning. This fits well with the growing
evidence of synaptic plasticity in the amygdala (see [45,46] 1.
48.
KIM
J, DECOLA JP, LANDER FERNANDEZ, FANXELOW S: N-
. .
Methyl-D-Aspartate Receptor Antagonist APV Blocks Acqui-
sition but not Expression of Fear Conditioning. Behall Neu-
rosci 1991, 105:16&167.
This study involves i.ltraventricular injection of 2~amino-5.phospho-
nopentanoate (Al%‘) and is thus ambiguous as to where the action oc-
curs. Together with the study by Miserendion et a(. [47**], however,
one can speculate that the effects occur in the amygdala. If so, the two
studies would support each other in implicating NMDA receptors in
fear conditioning.
49.
CHAPMANPF,
BELLAVANCEL.:
nduction of Long-Term Poten-
. .
tiation in the Basolateral Amygdala does not Depend on
NMD A Receptor Activation. Synapse 1992, in press.
This study is potentially damaging to the hypothesis that synaptic plas
ticity
in the amygdala underlies emotional learning, and that both synap-
tic plasticity and emotional learning depend upon NMDA receptors (see
[47**] ). This is not the only form of LTP that has been demonstrated
in the amygdala, however, and the findings only show that this form
is independent of NMDA receptors. It is still possible Fiat an NMDA~
dependent form of LTP will be found. Regardless. Of, the mechanism,
amygdala LTP is a new and exciting research a& th% bffefs new pos-
sibilities in understanding cellular mechanis,??
of
e onal memory
and in relating synaptic plasticity to normal;raemory processes.
JE LeDoux, Center for Neural Science, New York University, 6 Wash-
ington Place, New York, New York 10003, USA.
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