2.14 - Evolution of the Amygdala in Vertebrates

Abstract

The main aim of this article is to identify the homologues of the different components of the mammalian amygdala in the cerebral hemispheres of non-mammals using, primarily, a topological/embryological perspective. Thus, we first consider two main divisions of the amygdala of mammals, namely the pallial and subpallial (striatopallidal) amygdala. The pallial amygdala includes derivatives of both the lateral and ventral embryonic pallium that in the adult conform layered, superficial areas usually called cortical amygdala, and deep nuclei that conform the basolateral division of the amygdala plus the amygdalohippocampal area (AHA). The components of the subpallial amygdala are usually grouped in two divisions known as central (central amygdala plus parts of the bed nucleus of the stria terminalis, BST) and medial (medial amygdala plus the posteromedial BST) extended amygdala (EA). We then characterize each of the pallial and subpallial components of the mammalian amygdala using neurochemical and hodological data from the literature. After dissecting out and characterizing the amygdaloid centers of mammals, we use the same criteria (topological/embryological, neurochemical, and hodological) to identify the different components of the reptilian amygdala. This approach reveals that the cortical amygdala of reptiles is composed of the nucleus sphericus and the ventral anterior amygdala, plus maybe portions of the caudal lateral cortex. The reptilian basolateral amygdala includes the posterior dorsal ventricular ridge and the dorsolateral amygdaloid nucleus. In addition, the ventral posterior amygdala seems the reptilian homologue of the mammalian AHA. As in mammals, centers in the subpallial amygdala of reptiles conform a central (striatoamygdaloid transition area and dorsolateral BST) and medial (medial amygdala plus the ventromedial BST) EA. The strong similarities between the avian and reptilian cerebral hemispheres allow us to make a proposal for the identity of the amygdala and its components in the avian telencephalon. This proposal, which nicely fits the embryological/topological, hodological, and neurochemical criteria used to define the divisions of the mammalian amygdala, suggests that the avian amygdala is much larger than previously believed. Whereas in birds the cortical amygdala is reduced to a small rim of olfacto-recipient tissue in the caudal cerebral hemispheres (posterior cortex piriformis plus the surface of the rostral arcopallium), the avian basolateral amygdala consists of the rest of the arcopallium and most of the caudal nidopallium. In addition, the posterior amygdala is the best candidate for the avian homologue of the AHA of mammals. Finally, the nonpallial centers of avian amygdala can also be grouped into a central (SpA and lateral BST) and a medial (nucleus teniae and medial BST) EA. This thorough comparative analysis suggests that the amygdala is an ancient component of the cerebral hemispheres of tetrapods that includes two functional subsystems, namely the central/basolateral and the medial subsystem (which includes the medial EA and the AHA), involved in managing two different, but closely related, functions. The central/basolateral subsystem coordinates innate and learned reactions of fear/anxiety/aversion (through the descending projections of the central EA) or of attraction/reward-directed behaviors (through its projections to the striatum) to virtually any stimulus. The medial subsystem is primarily involved in the coordination of species-specific behavioral responses to chemosensory stimuli (olfactory and vomeronasal) with a strong emotional component, such as reproductive behaviors, defensive/aggressive behaviors to conspecifics (agonistic behaviors), or to predator-derived chemosignals. The deep interconnections of both subsystems explain why reproductive-agonistic behaviors are strongly emotional and might mediate learned emotional responses to many odorants.