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

Abstract

In a recent study, we tentatively identified different subdivisions of the central extended amygdala (EAce) in chicken based on the expression of region-specific transcription factors (including Pax6 and Islet1) and several phenotypic markers during embryonic development. Such a proposal was partially based on the suggestion that, similarly to the subdivisions of the EAce of mammals, the Pax6 and Islet1 neurons of the comparable chicken subdivisions derive from the dorsal (Std) or ventral striatal embryonic domains (Stv), respectively. To investigate whether this is true, in the present study, we carried out cell migration assays from chicken Std or Stv combined with immunofluorescence for Pax6 or Islet1. Our results showed that the cells of the proposed chicken EAce truly originate in either Std (expressing Pax6) or Stv (expressing Islet1). This includes lateral subdivisions previously compared to the intercalated amygdalar cells and the central amygdala of mammals, also rich in Std-derived Pax6 cells and/or Stv-derived Islet1 cells. In the medial region of the chicken EAce, the dorsal part of the lateral bed nucleus of the stria terminalis (BSTL) contains numerous cells expressing Nkx2.1 (mostly derived from the pallidal domain), but our migration assays showed that it also contains neuron subpopulations from the Stv (expressing Islet1) and Std (expressing Pax6), resembling the mouse BSTL. These findings, together with those previously published in different species of mammals, birds and reptiles, support the homology of the chicken EAce to that of other vertebrates, and reinforce the existence of several cell subcorridors inside the EAce. In addition, together with previously published data on neuropeptidergic cells, these results led us to propose the existence of at least seventeen neuron subtypes in the EAce in rodents and/or some birds (chicken and pigeon). The functional significance and the evolutionary origin of each subtype needs to be analyzed separately, and such studies are mandatory in order to understand the multifaceted modulation by the EAce of fear responses, ingestion, motivation and pain in different vertebrates.

Multiple amygdaloid divisions of arcopallium send convergent projections to the nucleus accumbens and neighboring subpallial amygdala regions in the domestic chicken: a selective pathway tracing and reconstruction study

“…While BSTL develops in the pallidal domain of the forebrain, Ac is a ventral striatal derivative. According to Vicario et al (2015), the amount of Islet1 (taken as a marker for the ventral striatal domain) was significant, mainly in the dorsomedial BSTL but also visible in the dorsolateral subregion, interspersed with Pax6 and Nkx.2.1., pointing to a potential ‘overflow’ from Ac. The area defined SpAr may also encroach upon territories of Ac shell [Alheid et al 1995; de Olmos et al 2004), see further discussion of the question by Alba Vicario, doctoral thesis (2015)].…”

“…In the course of development, these neurons originating from subpallial (medial ganglionic eminence, lateral ganglionic eminence, preoptic) and pallial (esp. ventral pallial) primordia followed specific migratory routes or cell subcorridors (Vicario et al 2015), e.g., the stria terminalis. Because of migration, cellular clusters originating from one domain may invade the territories of other domains, rendering the borders ‘fuzzy’.…”

“…For example, a recently described calcium binding protein, secretagogin, known to occur in EA regions of mammals (Mulder et al 2010) labels clusters of selected neurons also in the subpallial amygdala, including BSTL, of domestic chickens, whereas the Ac (together with the striatal complex) are impoverished in secretagogin label (Gati et al 2014). Based on a detailed study on specific transcription factors and cell tracking in chicken (Vicario et al 2015), the BSTLd (as defined in the paper) contains neurons of both pallidal and striatal origin. While BSTL develops in the pallidal domain of the forebrain, Ac is a ventral striatal derivative.…”

Genoarchitecture of the extended amygdala in zebra finch, and expression of FoxP2 in cell corridors of different genetic profile

“…In mammals, the EAme is particularly relevant for aspects of social behavior related to affiliation, agonistic behavior (including aggresion/defense) and sexual behavior (Choi et al 2005; Hammock and Young 2006), while the EAce is essential for fear/anxiety responses and reward (Davis 1992; Walker et al 2003; Kalin et al 2004; Phelps and LeDoux 2005; Walker and Davis 2008; Walker et al 2009; Davis et al 2010; reviewed by Martínez-García et al 2007, 2012), and is also relevant for modulating some of the emotional aspects that drive social behavior (Moore and Isen 1990). Both parts of the extended amygdala have been recently redefined in mice and chickens based on expression of transcription factors during development and the embryonic origin of their neurons (mouse: García-López et al 2008; Bupesh et al 2011a, b; chicken: Abellán and Medina 2009; Abellán et al 2013; Vicario et al 2014, 2015). Multiple embryonic domains produce neurons for the EAce and EAme.…”

“…Multiple embryonic domains produce neurons for the EAce and EAme. Neurons produced in each distinct domain are characterized by specific genetic profiles and distribute, by way of radial or tangential migrations, along the extended amygdala, forming corridors of cells with a similar phenotype that are apparently enrolled in a similar functional pathway (reviewed by Abellán et al 2013 for the EAme; see Bupesh et al 2011b, and Vicario et al 2014, 2015, for the EAce). These data open a new venue for trying to understand the functional organization of the extended amygdala, and the multifaceted modulation of social behavior by this complex structure.…”