The amygdala controls emotional and social behavior and regulates instinctive reflexes such as defense and reproduction by way of descending projections to the hypothalamus and brainstem. The descending amygdalar projections are suggested to show a cortico-striato-pallidal organization similar to that of the basal ganglia (Swanson [2000] Brain Res 886:113-164). To test this model we investigated the embryological origin and molecular properties of the mouse centromedial and extended amygdalar subdivisions, which constitute major sources of descending projections. We analyzed the distribution of key regulatory genes that show restricted expression patterns within the subpallium (Dlx5, Nkx2.1, Lhx6, Lhx7/8, Lhx9, Shh, and Gbx1), as well as genes considered markers for specific subpallial neuronal subpopulations. Our results indicate that most of the centromedial and extended amygdala is formed by cells derived from multiple subpallial subdivisions. Contrary to a previous suggestion, only the central--but not the medial--amygdala derives from the lateral ganglionic eminence and has striatal-like features. The medial amygdala and a large part of the extended amygdala (including the bed nucleus of the stria terminalis) consist of subdivisions or cell groups that derive from subpallial, pallial (ventral pallium), or extratelencephalic progenitor domains. The subpallial part includes derivatives from the medial ganglionic eminence, the anterior peduncular area, and possibly a novel subdivision, called here commissural preoptic area, located at the base of the septum and related to the anterior commissure. Our study provides a molecular and morphological foundation for understanding the complex embryonic origins and adult organization of the centromedial and extended amygdala.
Here we studied the combinatory expression patterns of nine developmental regulatory genes and six markers of different neuronal subpopulations in the telencephalic subpallium of developing chicken, from early embryos until hatching, in order to better understand the formation and organization of the basal telencephalon and the origin of its different cell groups. The genes analyzed include those encoding for: the transcription factors Islet1, Lhx6, Lhx7/8, Nkx2.1, and Pax6; the signaling protein Sonic hedgehog; the LIM-only genes Lmo3 and Lmo4; the cell adhesion molecule cadherin-8; markers of gamma-aminobutyric acid (GABA)ergic, cholinergic, or glutamatergic neurons; and markers of neuron subpopulations containing substance P, enkephalin, or neuropeptide Y. The combinatory expression patterns of these genes indicate that the chicken subpallium parcellates into eight molecularly different compartments during development (three striatal, three pallidal, and two preoptic subdivisions), and suggest that each compartment produces specific cell groups. Our data are particularly relevant for understanding the avian extended amygdala and suggest the existence of distinct central and medial extended amygdala complexes in the subpallium, as well as a pallial amygdalo-hypothalamic cell corridor, which are comparable to homonymous complexes of mammals based on similar embryonic origin, molecular features, and some connectivity patterns. Our data also indicate that the dorsal and ventral parts of the chicken basal ganglia originate in different striatal and pallidal compartments, and suggest a massive migration of neurons from the pallidal compartment into the medial striatum, which may explain the existence of pallidal-like cells within the medial striatum of birds.
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