What is the amygdala? A comparative approach
Authors: Enrique Lanuza, Alino Martı́nez-Marcos, Fernando Martı́nez-Garcı́a
Journal: Trends in Neurosciences (1999)

In their exciting and provocative article1Swanson L.W. Petrovich G.D. Trends Neurosci. 1998; 21: 323-331Abstract Full Text Full Text PDF PubMed Scopus (1121) Google Scholar, Swanson and Petrovich consider the term ‘amygdala‘ to be an arbitrary name describing a series of structures that are heterogeneous from both anatomical and functional viewpoints. Functionally, they see the amygdala as being made up of nuclei that belong to the autonomic nervous system (central nucleus), the vomeronasal system (medial, posteromedial cortical and posterior nuclei), the olfactory system (the cortical olfactorecipient nuclei, the basomedial nucleus and the posterior part of the basolateral nucleus) and the frontotemporal cortical system (lateral nucleus and anterior basolateral nucleus). Anatomically, they consider the amygdala to be composed of traditional cortical (cortical nuclei and areas receiving direct olfactory input), claustral (basolateral amygdala) and striatal elements (central and medial nuclei). In the past, a combination of different methods has demonstrated the role of the basolateral and central amygdala in fear conditioning and emotional learning2Davis M. Int. Rev. Neurobiol. 1994; 36: 225-266Crossref PubMed Scopus (156) Google Scholar, 3Ono T. Nishijo H. Uwano T. Prog. Neurobiol. 1995; 46: 401-422Crossref PubMed Scopus (116) Google Scholar, 4LeDoux J.E. The Emotional Brain. Simon & Schuster, 1996Google Scholar. Therefore, the basolateral amygdala (frontotemporal) and the central amygdala (autonomic) appear to constitute a single functional system that, according to anatomical data from reptile studies5Bruce L.L. Neary T.J. Brain Behav. Evol. 1995; 46: 224-234Crossref PubMed Scopus (255) Google Scholar, 6Lanuza E. et al.J. Comp. Neurol. 1997; 384: 537-555Crossref PubMed Scopus (51) Google Scholar, 7Lanuza E. et al.Eur. J. Neurosci. 1998; 10: 3517-3534Crossref PubMed Scopus (64) Google Scholar, appears to have been well conserved during vertebrate evolution. Although the remaining amygdaloid nuclei certainly belong to the main and accessory olfactory systems (in view of the large number of afferents from the olfactory bulbs), even Swanson and Petrovich recognize that they have a set of intricate interconnections with the central and basolateral amygdala. The activity in the chemosensory amygdala must, therefore, have a strong influence on the basolateral and central amygdala, which suggests a functional interdependence of all the amygdaloid nuclei. Additionally, as is emphasized by the authors1Swanson L.W. Petrovich G.D. Trends Neurosci. 1998; 21: 323-331Abstract Full Text Full Text PDF PubMed Scopus (1121) Google Scholar, their structural classification of the amygdala coincides essentially with that proposed by Johnston in 1923 (8Johnston J.B. J. Comp. Neurol. 1923; 35: 337-482Crossref Scopus (422) Google Scholar). Using a comparative perspective, Johnston divided the amygdala into a primitive group of nuclei, which includes the ‘striatal’ and ‘olfactory’ nuclei, and a phylogenetically new group of nuclei, the ‘claustral’ amygdala. However, recent connectional and neurochemical studies have revealed the presence of a putative homologue to the mammalian basolateral amygdala in the dorsal ventricular ridge (DVR) of the reptilian brain5Bruce L.L. Neary T.J. Brain Behav. Evol. 1995; 46: 224-234Crossref PubMed Scopus (255) Google Scholar, 6Lanuza E. et al.J. Comp. Neurol. 1997; 384: 537-555Crossref PubMed Scopus (51) Google Scholar, 7Lanuza E. et al.Eur. J. Neurosci. 1998; 10: 3517-3534Crossref PubMed Scopus (64) Google Scholar, which, following the view held by Swanson and Petrovich, would be claustral and, therefore, isocortical in nature. Were this true, the DVR would represent the reptilian counterpart of the claustrum9Striedter G.F. Brain Behav. Evol. 1997; 49: 179-213Crossref PubMed Scopus (239) Google Scholar and other derivatives of the cortical cell plate (layer VIb), even though the remaining layers of the isocortex are absent in the reptilian brain. However, the reptilian DVR has a subcortical origin10Yanes C.M. et al.J. Morphol. 1987; 194: 55-64Crossref Scopus (13) Google Scholar, 11Lohman A.H.M. Smeets W.J.A.J. Finley B.L. Innocenti G. Scheich H. The Neocortex. Plenum Press, 1990: 59-74Google Scholar and occupies a subventricular position in the adult. This strongly suggests that the basolateral amygdala is not a cortical (claustral) structure. Data on the expression of genes that control regional specification, morphogenesis and differentiation in the forebrain of embryonic vertebrates are urgently needed in order to clarify this issue. The major legacy of Johnston's work on the amygdala is not the compartmentalization he proposed but the use of a comparative perspective, which is essential to elaborate solid hypotheses concerning the anatomical and functional organization of the brain. ReplySwanson et al.Trends in NeurosciencesMay 01, 1999In Brief Full-Text PDF