Subdivisions and derivatives of the chicken subpallium based on expression of LIM and other regulatory genes and markers of neuron subpopulations during development

Abstract

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 -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. J. Comp. Neurol. 515:465–501, 2009.

Grant sponsor: the Spanish Ministry of Education and Science—Fondo Europeo de Desarrollo Regional (FEDER); Grant numbers: BFI2003-06453- C02-02 and BFU2006-14804-C02-02/BFI (to L.M.). Predoctoral fellowship to A.A.