The Olfactory Amygdala in Amniotes: An Evo‐Devo Approach

Abstract

In tetrapods, the medial amygdala is a forebrain center that integrates olfactory and/or vomeronasal signals with the endocrine and autonomic systems, playing a key role in different social behaviors. The vomeronasal system has undergone important changes during evolution, which may be behind some interspecies differences in chemosensorymediated social behavior. These evolutionary changes are associated with variations in vomeronasal-recipient brain structures, including the medial amygdala. Herein, we employed an evolutionary developmental biology approach for trying to understand the function and evolution of the medial amygdala. For that purpose, we reviewed published data on fate mapping in mouse, and the expression of orthologous developmental regulatory genes (Nkx2.1, Lhx6, Shh, Tbr1, Lhx9, Lhx5, Otp, and Pax6) in embryos of mouse, chicken, emydid turtles, and a pipid frog. We also analyzed novel data on Lhx9 and Otp in a lacertid lizard. Based on distinct Abbreviations used: AAv 5 anterior amygdala, ventral part; ACo 5 anterior cortical amygdalar area; AHN 5 anterior hypothalamic nucleus; AOB 5 accessory olfactory bulb; AON 5 anterior olfactory nucleus; APH 5 parahippocampal area (chicken); Arc 5 arcopallium (part of the pallial amygdala in chicken); AStr 5 amygdalo-striatal transition area; BAOT 5 bed nucleus of the accessory olfactory bulb; Bas 5 basal nucleus (Meynert); BC 5 basal amygdalar complex; BL 5 basolateral amygdalar nucleus; BLA 5 basolateral amygdalar nucleus, anterior part; BLV 5 basolateral amygdalar nucleus, ventral part; BM 5 basomedial amygdalar nucleus; BMA 5 basomedial amygdalar nucleus, anterior part; BSTia 5 bed nucleus of the stria terminalis, intraamygdaloid part; BSTM 5 bed nucleus of the stria terminalis, medial part; BSTM1 5 dorsolateral subnucleus of BSTM (chicken); BSTM2 5 ventromedial subnucleus of BSTM (chicken); CDL 5 dorsolateral corticoid area (chicken); Ce 5 central amygdala (central amygdalar nucleus); Co 5 cortical amygdalar area (chicken, comparable to ACo of mammals); CPu 5 caudate-putamen; CxA 5 cortico-amygdalar transition area; DC 5 dorsal cortex (reptile); DEn 5 dorsal endopiriform nucleus; EMT 5 prethalamic (or thalamic) eminence; Ent 5 entorhinal cortex; Gaba1 5 g-aminobutyric acid (GABA)-ergic cells; Glu1 5 glutamatergic cells; GP 5 globus pallidus; GPL 5 globus pallidus, lateral part; GPM 5 globus pallidus, medial part; Hb 5 basal hypothalamus; Hip 5 hippocampal formation, rostral olfacto-recipient part; I 5 intercalated cell groups of the amygdale; ic 5 internal capsule; IM 5 intercalated cell groups of the amygdala, main division; L 5 lateral amygdalar nucleus; LC 5 lateral cortex (reptile); LGE 5 lateral ganglionic eminence; LOT 5 nucleus of the lateral olfactory tract; LOT1 5 nucleus of the lateral olfactory tract, layer 1; MC 5 medial cortex (reptile); Me 5 medial amygdala in nonmammals; MeA 5 medial amygdala, anterior part; MeAV 5 medial amygdala, anteroventral part; MePD 5 medial amygdala, posterodorsal part; MePV 5 medial amygdala, posteroven...

Embryonic Origin of the Islet1 and Pax6 Neurons of the Chicken Central Extended Amygdala Using Cell Migration Assays and Relation to Different Neuropeptide-Containing Cells

“…Although more studies are needed to further investigate the distribution, molecular profile and connections of the neurons in each subcorridor, with the available data it is tempting to suggest that neurons with the same origin along each subcorridor of the EAce share many molecular and connectivity features, and are possibly involved in the same functional network. A similar suggestion has been raised for neurons of distinct embryonic origin of the medial extended amygdala [García-López et al, 2008;Bupesh et al, 2011b;Medina et al, 2011;Medina and Abellán, 2012;Sokolowski and Corbin, 2012;Abellán et al, 2013]. If proven, developmental data may become essential for helping to unravel the otherwise extremely complex chemical and hodological organization of the EAce, and for understanding its involvement in so many, multifaceted functions (fear/anxiety, feeding/satiety, reward/aversion and pain/analgesia).…”

“…In recent years, the embryonic commissural PO, characterized by expression of Nkx2.1, Shh and Lhx7 at the ventricular zone and mantle, has emerged as a major source of neurons for the medial extended amygdala (mouse: García-López et al [2008], Carney et al [2010] and Bupesh et al [2011b] and chicken: Me-dina [2008, 2009] and reviews by Medina et al [2011] and Abellán et al [2013]). More recently, the embryonic commissural PO was also shown to produce a minor subpopulation of catecholaminergic neurons for the EAce and St in mice [Bupesh et al, 2014], and a similar contribution was also suggested to occur in chicken ( fig.…”

Evolutionary and Developmental Contributions for Understanding the Organization of the Basal Ganglia

“…This is not surprising since the embryonic origin of any single neuron has a strong influence on its future chemical features, connections and physiological characteristics. In the mouse centromedial extended amygdala, which is highly heterogeneous regarding neuron constitution and embryonic origin, there is also a trend for neurons having the same origin to share similar chemical features and connections, and to be involved in similar functions [García-López et al, 2008;Bupesh et al, 2011a, b;Medina et al, 2011;Abellán et al, 2013]. Thus, developmental studies have provided key information for a better understanding of the functional anatomical organization of the globus pallidus in mammals.…”

“…Modern developmental studies using tools for analyzing gene expression, gene function and fate mapping help to understand the embryonic origin and basic features of each neuron subtype of the basal ganglia and other subpallial structures, such as the centromedial extended amygdala [Marín et al, 2000;García-López et al, 2008;Hirata et al, 2009;Carney et al, 2010;Nóbrega-Pereira et al, 2010;Bupesh et al, 2011a, b;Abellán et al, 2013]. In the centromedial amygdala, this information is key to unraveling its functional anatomical organization in mammals and to establish the basis for comparisons with other species [Moreno et al, 2009;Medina et al, 2011;Abellán et al, 2013].…”

“…In the centromedial amygdala, this information is key to unraveling its functional anatomical organization in mammals and to establish the basis for comparisons with other species [Moreno et al, 2009;Medina et al, 2011;Abellán et al, 2013]. We expect that such studies applied to the basal ganglia and done in different species in the light of evolutionary developmental biology [Wullimann and Mueller, 2004;Medina, 2009;Moreno et al, 2009] will be essential in order to be able to: (a) identify the same molecularly distinct progenitor zones that produce neurons for the basal ganglia nuclei in different species 1 ; (b) know whether basal ganglia nuclei in different species, if present, are formed by identical or partially different sets of neuron subpopulations (identified by their embryonic origin and transcription factor expression during development), and (c) identify possible mechanisms that may explain the evolution of the basal ganglia (for example, changes in the expression of developmental regulatory genes, and in the enhancers, activators, repressors and/or cofactors that regulate the expression), taking into account that evolution of morphological diversity is the consequence of nonlethal changes that occurred during development and were preserved by natural selection [Carroll et al, 2001;Medina, 2007].…”