The amygdala of the common shrew, guinea pig, rabbit, fox and pig: five flavours of the mammalian amygdala as a consequence of clade‐specific mosaic‐like evolution

Abstract

The amygdala is a part of neural networks that contribute to the regulation of emotional behaviours and emotional learning, stress response, and olfactory, pheromonal and reproductive functions. All these various functions are processed by the three main functional systems, frontotemporal, autonomic and olfactory, which are derived from different telencephalic sources (claustrum, striatum and olfactory cortex) and are represented, respectively, by the basolateral complex (BLC), the central complex (CC) and corticomedial complex (CMC) of the amygdala. The question arises of how these three functional systems evolved during mammalian phylogeny to fit the amygdala to specific needs of various animals. In the present study, we provide quantitative information regarding the individual volumes and neuron numbers in the BLC, CC and CMC of the common shrew, guinea pig, rabbit, fox and pig, a series of animals arranged according to increasing size and complexity of the brain. The results show that, in this series of animals, the BLC underwent a gradual size increase in volume and number of neurons, whereas the CMC was gradually reduced with regard to both these measures. The CC was more or less conserved across studied species. For example, the volume of the amygdala in pigs is 250 times larger than that in shrews and it also has almost 26 times as many neurons as the amygdala of shrews. However, the volumes of the BLC, CC and CMC were~380, 208 and 148 times larger, respectively, in pigs than in shrews. The number of neurons in these three regions was~38, 23 and 20 times greater, respectively, in pigs than in shrews. The results also show striking morphometric similarities of the amygdala in the guinea pig and rabbit as well as fox and pig. For example, the percentages of neurons in the fox and pig are 42.23% and 42.78%, respectively, for the BLC, 16.64% and 16.58%, respectively, for the CC, and 41.12% and 40.64%, respectively, for the CMC. In conclusion, our results indicate that the amygdala does not evolve as a single unit but, instead, the three main functional systems evolved independently, which suggests that brain structures with major functional links evolve together independently of evolutionary changes in other unrelated structures. The size progression of the BLC parallels the size progression of the neocortex with which it is strongly functionally linked, whereas the CMC is strongly connected to olfactory regions, and all these structures follow the same regression course. Remarkable morphometric similarity of the amygdala in the guinea pig and rabbit as well as in the fox and pig, however, suggest that there must also be another mechanism shaping the morphology of the amygdala and the brain during evolution. The gradual nature of size changes in the BLC and CMC support this hypothesis as well.

The evolutionary trajectories of the individual amygdala nuclei in the common shrew, guinea pig, rabbit, fox and pig: A consequence of embryological fate and mosaic‐like evolution

“…The anatomical boundaries of the amygdala and its various nuclei can be reliably defined across the studied species in Nissl stained sections, which was demonstrated in several of our previous papers (Równiak, 2013; Równiak & Bogus‐Nowakowska, 2020; Równiak et al, 2004). In the present study, the effect of such delineation in five studied species was visualized in 3‐D format to show the relationships among the individual amygdala nuclei (Figures 1 and 2).…”

“…Each of these species was analysed using six adult individuals. The average brain masses of these species were already reported in a previous study (Równiak & Bogus‐Nowakowska, 2020).…”

“…It includes several large and frequently investigated regions, such as the lateral (LA), basolateral (BL), basomedial (BM), cortical (CO), central (CE) and medial nuclei (ME), as well as some smaller and less well‐studied components, that is, the nucleus of the lateral olfactory tact (NLOT), the nucleus of the accessory olfactory tract (BAOT), anterior amygdaloid area (AAA), intra‐amygdaloid portion of the stria terminalis (BSTiA), intercalated nucleus (I) and amygdalohippocampal area (AHA) (Sah et al, 2003; Schröder et al, 2020; Swanson & Petrovich, 1998). All of these structures have been categorized and grouped by various researchers according to various concepts (Krettek & Price, 1978; LeDoux, 2007; Pabba, 2013; Richardson, 1973; Równiak & Bogus‐Nowakowska, 2020; Schröder et al, 2020; Stephan et al, 1987); however, in the context of amygdala evolution, the studies of Swanson and Petrovich (1998), Puelles et al (2000), Martínez‐García et al (2002), Medina et al (2004) and Garcia‐Calero et al (2020) are especially interesting.…”

“…There is also a neuroanatomical concept called the corticomedial amygdala which usually includes ME, CO, NLOT and BAOT and which represents the vomeronasal and olfactory regions of the amygdala (Kevetter & Winans, 1981a, 1981b; LeDoux, 2007; Richardson, 1973; Równiak & Bogus‐Nowakowska, 2020), however, it has a dual embryological origin (Swanson & Petrovich, 1998). A part of it is formed by ME which has mainly a subpallial origin (Bupesh et al, 2011; Puelles et al, 2000; Swanson & Petrovich, 1998).…”

“…Another part includes CO, NLOT and BAOT and is composed of derivatives of the olfactory cortex (ventral and lateral pallium) forming the caudal end of the piriform lobe (Moreno & González, 2007; Puelles et al, 2000; Swanson & Petrovich, 1998). The corticomedial amygdala, consisting of ME, CO, and NLOT, was often analysed as a consistent concept in various neuroanatomical studies (Crosby & Humphrey, 1944; Kevetter & Winans, 1981a; Równiak & Bogus‐Nowakowska, 2020) as all of these three regions have laminated cellular arrangement more or less similar to the piriform cortex, are interconnected, and have strong bidirectional connections with the main and accessory olfactory bulbs (Kevetter & Winans, 1981a, 1981b; Pitkänen et al, 2000). At present, the corticomedial amygdala is considered the main sensory gateway for olfactory and vomeronasal cues and it is the main region in the amygdala for processing reproductive and defensive behaviours (Gutiérrez‐Castellanos et al, 2010; Hong et al, 2014; Maras & Petrulis, 2008; Sah et al, 2003).…”