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 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.

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

“…Recent evidence on the development of the telencephalon in chicken and turtles has shown that the nucleus identified as globus pallidus in these animals is rich in Nkx2.1-expressing cells that appear to derive from a MGE-like embryonic domain (the pallidal embryonic subdivision; fig. 2 ) [Fernandez et al, 1998;Puelles et al, 2000;Cobos et al, 2001;Abellán and Medina, 2009;Moreno et al, 2010;Kuenzel et al, 2011]. Thus, the globus pallidus in sauropsids appears to contain at least the pallido/Nkx2.1 lineage cell type, expressing GABA, PV and LANT6, and with descending projections to the subthalamic nucleus and substantia nigra, comparable to a similar type found in the globus pallidus of rodents and primates ( table 1 ).…”

“…In addition to this major cell type, the globus pallidus in chicken also contains subpopulations of neurons expressing ppENK or SP+ mRNA [Abellán and Medina, 2009] ( table 1 ). The embryonic origin of these cells is unclear, but it is likely that they derive from the striatal progenitor (LGE-like) zone, as the projection neurons of the striatum (containing either ENK or SP) do [Abellán and Medina, 2009].…”

Changes in cortical interneuron migration contribute to the evolution of the neocortex

“…Lhx6 is a transcription factor that is specifically expressed in MGE cells (13), and the migration of MGE cells from the neocortical SVZ to the CP/MZ seems to be reduced at an early stage in the development of mouse Lhx6 null embryos (47,48). However, because Lhx6 is expressed in the chicken pallium in a dispersed manner (49) and thus, is likely to be expressed in chicken interneurons derived from the MGE, the downstream cascade of Lhx6 may have changed during mammalian evolution to enable the MGE-derived cells to enter the neocortical CP/MZ.…”

Contributions of Developmental Studies in the Dogfish <b><i>Scyliorhinus canicula</i></b> to the Brain Anatomy of Elasmobranchs: Insights on the Basal Ganglia

“…3 d of Rodríguez-Moldes, 2009]. Although the ventricular zone of the pallium appears to be the potential source for these Pax6 cells, more studies are needed to know if this is the only source, as reported in Xenopus [Moreno et al, 2008], or if they may derive in part from the dorsal subdivision of the LGE, as reported in amniotes [Puelles et al, 2000;Flames et al, 2007;Abellán and Medina, 2009;Moreno et al, 2010;Bupesh et al, 2011;Medina et al, 2011]. Whatever its origin, this stream of Pax6 cells may be a useful landmark in Scyliorhinus of the lateral margin of the LGE equivalent (developing striatum).…”

“…4 l) points to its probable pallial origin. However, other possible sources must also be considered, as it is known that in amniotes the amygdala receives Pax6-expressing cells from outside the telencephalon, including the thalamic eminence [Abellán and Medina, 2009;Bupesh et al, 2011]. This could be also possible in S. canicula , where the thalamic eminence also contains Pax6 cells [Rodríguez-Moldes, 2009] and a stream of these cells appears to extend between this diencephalic region and the amygdala-like subpallial region (open arrow in fig.…”