Subdivisions of the turtle Pseudemys scripta subpallium based on the expression of regulatory genes and neuronal markers

Abstract

The patterns of distribution of a set of conserved brain developmental regulatory transcription factors and neuronal markers were analyzed in the subpallium of the juvenile turtle, Pseudemys scripta. Immunohistochemical techniques were used with a combination of primary antibodies for the identification of the main boundaries and subdivisions in the basal telencephalon. In the basal ganglia, the combinatorial expression on Pax6, Nkx2.1, and GABA was a powerful tool for the identification of the nucleus accumbens, the dorsal portion of the striatum, and the pallidal regions. It was also possible to suggest migratory streams of neurons from the pallidum into the striatal regions. On the basis of GABA, Pax6, Tbr1, tyrosine hydroxylase, Darpp32, and Nkx2.1 combinatorial expression patterns, the boundaries of the septal subdivisions and their embryological origin were assessed. In particular, the bed nucleus of the stria terminalis was identified. Within the amygdaloid complex, the striatal central amygdala was characterized by Pax6 expression, whereas Orthopedia gene expression highlighted, at least, a subdivision of the medial amygdala. A newly identified preoptic commissural area and the boundaries of the preoptic area were assessed, mainly by the localization of Nkx2.1 expression. Finally, additional data were obtained by combining immunohistochemistry and tracing techniques on the interneuronal nature of the cholinerginergic, nitrergic, and Nkx2.1-positive striatal cells. Taken together, all the results of the present study allowed recognizing main features in the organization of the subpallium in reptiles that, in most cases, are shared with other amniotes and amphibians.

The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis

“…This reptilian homolog is neurochemically similar to the mammalian meAMY (Table 3) and contains sex steroid hormone receptors (Young et al, 1994;O'Connell et al, 2011c). Additionally, neurochemical evidence supports the subpallial origin of the reptilian meAMY (Table 3) (Moreno et al, 2010). Several functional studies into the role of the reptilian meAMY suggest that this region is also functionally similar to the mammalian meAMY and plays a conserved role in mediating aggression and courtship behavior.…”

“…Although some have proposed that the reptilian DVR is similar to the mammalian isocortex (Aboitiz, 1999), developmental studies have shown that the posterior DVR may be ventral pallial in origin (Fernandez et al, 1998;Puelles et al, 2000), whereas the mammalian isocortex is dorsal pallial in origin (Aboitiz et al, 2002). The posterodorsal DVR is positive for pallial markers Tbr-1 and Lhx9, while the dorsolateral amygdala is positive for the pallial markers Emx-1 and Tbr-1 (Fernandez et al, 1998;Moreno et al, 2010), further supporting the homology of these two reptilian regions to the mammalian blAMY. Finally, the dorsolateral amygdala has both dopaminergic and cholinergic innervation (Medina et al, 1993;Smeets, 1994), similar to the lateral pallial part of the mammalian blAMY (Loughlin and Fallon, 1984;Carlsen et al, 1985).…”

“…The reptilian BNST also contains neuropeptide-producing cells (Smeets et al, 1990), similar to mammals and birds. This region also has a similar developmental origin to the mammalian BNST, marked by Tbr-1, Dlx, Nkx2.1, and GAD67 expression (Table 3; Moreno et al, 2010). The BNST shares connections with the amygdala and hypothalamus, as well as many regions of the reward system .…”

“…blAMY: basolateral amygdala; BNST: bed nucleus of the stria terminalis; HIP: hippocampus; meAMY: medial amygdala; POA: preoptic area; STR: striatum. References: Mammals: Stoykova and Gruss, 1994;Gao and Moore, 1996;Fernandez et al, 1998;Eisenstat et al, 1999;Puelles et al, 2000;Tamamaki et al, 2003;Flames et al, 2007;Garcia-Lopez et al, 2008;Bird: Fernandez et al, 1998;Puelles et al, 2000;Bardet et al, 2010;Reptile: Fernandez et al, 1998;Metin et al, 2007;Moreno et al, 2010;Amphibians: Brox et al, 2003Gonzalez, 2007c, Moreno et al, 2008;Teleosts: Mueller et al, 2008;Alunni et al, 2004;Menuet et al, 2007;Mueller and Guo, 2009. specifically in this nucleus. However, female salamanders exposed to male pheromones show increased c-fos expression in this region (Laberge et al, 2008), suggesting a conserved role for this region in processing social olfactory information.…”

Proliferation, Migration, and Survival of Cells in the Telencephalon of the Ball Python, Python Regius

“…Currently, the mammalian, avian, and reptilian STR all appear to be hodologically, neurochemically, and developmentally similar (Gonzalez et al, 1990;Moreno et al, 2010;Russchen and Jonker, 1988;Smeets, 1988;Smeets et al, 1986;Smeets et al, 1987). Lesioning the reptilian STR in male A. carolinensis causes a reduction in male-typical assertation display (Greenberg, 1977).…”