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What Is the Amygdala? G.V. Wallenstein et al. – Hippocampal association V IEWPOINT Selected references in Computational Neuroscience (Bower, J.M., ed.), pp. 547–552, 1 Scoville, W.B. and Milner, B. (1957) J. Neurol. Neurosurg. Plenum Press Psychiatry 20, 11–21 31 Amaral, D.G. and Witter, M.P. (1989) Neuroscience 31, 571–591 2 O’Keefe, J. and Nadel, L. (1978) The Hippocampus as a Cognitive 32 Levy, W.B. (1989) in Computational Models of Learning in Simple Map, Oxford University Press Neural Systems (Hawkins, R.D. and Bower, G.H., eds), pp. 243–305, 3 Squire, L.R. (1992) Psychol. Rev. 99, 195–231 Academic Press 4 Eichenbaum, H. et al. (1994) Behav. Brain Sci. 17, 449–518 33 Wallenstein, G.V. and Hasselmo, M.E. (1997) Brain Res. Bull. 5 Rawlins, J.N.P. (1985) Behav. Brain Sci. 8, 479–496 43, 485–493 6 Cohen. N.J. and Eichenbaum, H. (1993) Memory, Amnesia, and 34 Nadel, L. and Willner, J. (1980) Physiol. Psychol. 8, 218–228 the Hippocampal System, MIT Press 35 Nadel, L. et al. 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(1987) Trends Neurosci. 49 Larson, D. et al. (1986) Brain Res. 368, 347–350 10, 408–415 50 Mott, D.D. and Lewis, D.V. (1991) Science 252, 1718–1720 22 Hasselmo, M.E. and Bower, J.M. (1993) Trends Neurosci. 16, 51 Bunsey, M. and Eichenbaum, H. (1996) Nature 379, 255–257 218–222 52 Dusek, J.A. and Eichenbaum, H. (1997) Proc. Natl. Acad. Sci. Acknowledgements 23 Hasselmo, M.E. (1993) Neural Comput. 5, 32–44 U. S. A. 94, 7109–7114 This work was 24 Hasselmo, M.E. (1995) Behav. Brain Res. 67, 1–27 53 Otto, T. and Eichenbaum, H. (1992) Hippocampus 2, 323–334 supported in part 25 Kleinfeld, D. (1986) Proc. Natl. Acad. Sci. U. S. A. 83, 9469–9473 54 Zhu, X.O. et al. (1995) Eur. J. Neurosci. 7, 753–765 by the Human 26 Kleinfeld, D. and Sompolinsky, H. (1988) Biophys. J. 54, 55 Hampson, R.E. et al. (1993) Behav. Neurosci. 107, 715–739 1039–1051 56 Deadwyler, S.A. et al. (1996) J. Neurosci. 16, 354–372 Frontier Science 27 Levy, W.B. (1996) Hippocampus 6, 579–590 57 Gothard, K.M. et al. (1996) J. Neurosci. 16, 823–835 Program and the 28 Jensen, O. and Lisman, J.E. (1996) Learn. Mem. 3, 279–287 58 Stevens, R. and Cowey, A. (1972) Brain Res. 46, 1–22 National Institutes 29 Wallenstein, G.V. and Hasselmo, M.E. (1997) J. Neurophysiol. 59 Reilly, S. et al. (1993) Behav. Neurosci. 107, 996–1004 78, 393–408 60 Yamamoto, T. et al. (1995) Neurosci. Res. 22, 31–49 of Mental Health 30 Wallenstein, G.V. and Hasselmo, M.E. (1997) in Advances 61 Mizumori, S.J.Y. et al. (1989) J. Neurosci. 9, 3915–3928 (MH-52732-04). What is the amygdala? Larry W. Swanson and Gorica D. Petrovich ‘Amygdala’ and ‘amygdalar complex’ are terms that now refer to a highly differentiated region near the temporal pole of the mammalian cerebral hemisphere. Cell groups within it appear to be differentiated parts of the traditional cortex, the claustrum, or the striatum, and these parts belong to four obvious functional systems – accessory olfactory, main olfactory, autonomic and frontotemporal cortical. In rats, the central nucleus is a specialized autonomic-projecting motor region of the striatum, whereas the lateral and anterior basolateral nuclei together are a ventromedial extension of the claustrum for major regions of the temporal and frontal lobes.The rest of the amygdala forms association parts of the olfactory system (accessory and main), with cortical, claustral and striatal parts.Terms such as ‘amygdala’ and ‘lenticular nucleus’ combine cell groups arbitrarily rather than according to the structural and functional units to which they now seem to belong.The amygdala is neither a structural nor a functional unit. Trends Neurosci. (1998) 21, 323–331 Larry W. Swanson and Gorica D. Petrovich are part LICES THROUGH THE TEMPORAL POLE of the entiation in the amygdala; and the extent of its outer of the Neuroscience Shuman cerebral hemispheres reveal an almond- border, and number and classification of its sub- Program at the shaped mass of gray matter that Burdach1 discovered divisions, remain controversial today. In this article, University of and called the amygdalar nucleus in the early 19th we present a model of amygdalar architecture based Southern century (Fig. 1). Starting about 50 years later, the on recent embryological, neurotransmitter, connec- California, microscopic examination of histological tissue sec- tional and functional data. When placed in the con- Los Angeles, CA tions began to reveal more and more structural differ- text of cerebral hemisphere architecture as a whole, 90089-2520, USA. Copyright © 1998, Elsevier Science Ltd. All rights reserved. 0166 - 2236/98/$19.00 PII: S0166-2236(98)01265-X TINS Vol. 21, No. 8, 1998 323 V IEWPOINT L.W. Swanson and G.D. Petrovich – What is the amygdala? the results suggest that, however defined today, ‘amygdala’ and ‘amygdalar complex’ refer to an arbitrarily defined set of cell groups. Historical background Meynert’s claim in 1867 that the amygdala of Burdach is a ventral, temporal lobe extension of the claustrum (according to Meynert the deepest layer of cortex)3 sparked a more than 50 year con- troversy about how to classify the amygdala in terms of basic parts of the cerebral hemisphere (telen- cephalon, endbrain). Equally dis- tinguished neuroanatomists soon proposed, instead, that the amyg- dala is part of the lenticular nucleus (a gross anatomical term Fig. 1. The first illustrations of the ‘amygdalar nucleus’ (Mandelkern), in the human cerebral hemisphere. An arrow has been added to the outline drawing on the right to indicate the amygdalar nucleus as drawn by Burdach. for the globus pallidus and puta- Comparison with a standard modern textbook (see Figs 66 and 92 in Ref. 2) shows that Burdach was referring to the men – two different cell groups in basolateral complex. Later workers added adjacent olfactory cortex, and the medial and central nuclei, to form the the basal nuclei or ganglia, rather ‘amygdalar complex’, which has been extended recently to include the bed nuclei of the stria terminalis (BST) and parts than in the cortex), and observed of the substantia innominata. Reproduced, with permission, from Ref. 1. that the amygdala is rimmed ventrally by olfactory cortex of the piriform lobe4. In 1923, J.B. Johnston5 introduced the fundamental description of amygdalar structure in widest use today, based on detailed analysis of com- parative vertebrate material. He proposed that the amygdala is divided into a primitive group of nuclei associated with the olfactory system (central, medial and cortical nuclei, and nucleus of the lateral olfactory tract), and a phylogenetically new group of nuclei (lateral and basal). Interest in classifying the amygdala and its various parts in terms of cerebral hemisphere subdivisions and phylogeny waned in the last 50 years as attention shifted to determining input/output relationships of each neuronal group, and the neurotransmitter/recep- tor systems contained within these pathways. Currently available data are much more extensive and reliable than those available to Johnston, and when taken together suggest that the amygdala is a hetero- geneous region, one part of which is a specialized ven- tromedial expanse of the striatum (central and medial nuclei, and anterior area), a second part of which is caudal olfactory cortex (nucleus of the lateral olfactory tract, cortical nucleus, and postpiriform and piriform– amygdalar areas), and a third part of which is a ventro- medial extension of the claustrum (lateral, basal and posterior nuclei).
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