Evolutionary development of the amygdaloid complex

In the early 19th century, Burdach discovered an almond-shaped mass of gray matter in the anterior portion of the mammalian temporal lobe, which he called “amygdala” (Burdach, 1819–1822). The first anatomical description of the amygdala was made in 1867 by Meynert (1867). Subsequently, a large number of other nuclei were added to the amygdala to constitute what is now known as the “amygdaloid complex” (AC) (Johnston, 1923). Until this day, AC remains a subject of intense investigation in terms of content and evolutionary development since it is a much more complicated structure than what was previously thought. It is therefore, important to know the evolutionary developmental origin of AC before we can completely understand its function. The AC is a multinuclear complex comprised of 13 nuclei. These nuclei are divided into three major groups: the basolateral, cortical-like, and centromedial. Other accessory nuclei such as the intercalated cell masses (I) and the amygdalo-hippocampus area have also been described. The basolateral group is comprised of the lateral nucleus (LA), basal nucleus (B), and accessory basal nucleus (AB) (Johnston, 1923). The cortical-like group of nuclei includes the nucleus of the lateral olfactory tract (NLOT), bed nucleus of the accessory olfactory tract (BAOT), anterior and posterior cortical nuclei (CoA and CoP, respectively), and periamygdaloid cortex (PAC). The centromedial nucleus consists of the central nucleus (CeA), medial nucleus (M), and amygdaloid part of the bed nucleus of stria terminalis (BST). The major remaining groups of AC are the amygdalohippocampal area (AHA) and intercalated nuclei (I) (Aggleton, 2000; Sah et al., 2003). These different nuclei of AC are connected within and also with various brain regions, and thus, process various types of information (e.g., olfactory and Figure 1A). Swanson and Petrovich (1998) definition of amygdala as neither a structural nor a functional unit provides an attractive point to explore the evolutionary developmental aspects of AC because a growing number of evidence suggests AC as an evolutionarily conserved structure. Earlier, research on structural organization of AC in different amniotic vertebrates revealed a common pattern of organization, along with shared functional roles. Conversely, research on anamniotes provided little comparative information regarding structural organization of AC. However, recent studies have shown a homology between amygdaloid components of amniotes and anamniotes. To better understand the evolutionary and developmental history of a particular brain region, one needs to follow a “sequential (step by step) approach,” which takes into account the developmental, topological, hodological, genetical, and functional history. Interestingly, recent data on AC of mammals, reptiles, and anurans suggest that the evolution of AC occurred as common traits of telencephlon, for example, regions of cortical amygdala such as nLOT and accessory olfactory bulb (AOB) (Remedios et al., 2007; Huilgol et al., 2013); but not as the sum of unrelated structures with different origins. The present understanding of AC in developmental and adult vertebrates suggests two major divisions of telencephlon: the pallium and the subpallium (Puelles et al., 2000; Martinez-Garcia et al., 2002; Moreno and Gonzalez, 2007b; Remedios et al., 2007). This dual view or origin makes AC a histogenetic complex structure of the adult brain, with extremely intense morphogenetic and migratory processes during the development in all tetrapods (Puelles et al., 2000). In mammals, the pallial component is composed of “cortical amygdala” and “basolateral amygdala.” In turn, the subpallial component consists of the striatal component, central amygdala, and medial amygdala. This basic plan is shared by reptiles, birds, and also by anuran amphibians (MartinezGarcia et al., 2002; Medina et al., 2004). Interestingly, this basic description is possible only in few mammalian tetrapods, but not in the non-mammalian amniotes and the anurans where they have no clear anatomical subdivisions. The existence of shared embryological AC components in all tetrapods provides clues to the presence of precursors of the amygdaloid nuclei from anamniotes (Moreno and Gonzalez, 2007b). The following sections deal with the current view on accepted and shared components of AC in tetrapods. The amygdala is a part of a phylogentically conserved olfactory system, particularly the olfactory bulb, in vertebrate evolution in terms of embryological origin, neurochemistry, connectivity, and function (MartinezGarcia et al., 2002; Huilgol et al., 2013). Additionally, a major part of amygdala is also an integral component of the vomeronasal system of the tetrapod (except avian) brain (Swanson and Petrovich, 1998; Moreno and Gonzalez, 2005a). In mammals, the vomeronasal information passes via the AOB to medial (MeA) and cortical postero-medial amygdala (CoApm) (Swanson and Petrovich, 1998). In addition, the amygdala also receives information from the main olfactory bulb (MOB) and hypothalamus to modulate reproductive and defensive behaviors (Canteras et al., 1995). In reptiles and anurans, the existence of a well-developed “vomeronasal amygdala”