Expression of regulatory genes in the embryonic brain of a lizard and implications for understanding pallial organization and evolution

Abstract

The comparison of gene expression patterns in the embryonic brain of mouse and chicken is being essential for understanding pallial organization. However, the scarcity of gene expression data in reptiles, crucial for understanding evolution, makes it difficult to identify homologues of pallial divisions in different amniotes. We cloned and analyzed the expression of the genes Emx1, Lhx2, Lhx9, and Tbr1 in the embryonic telencephalon of the lacertid lizard Psammodromus algirus. The comparative expression patterns of these genes, critical for pallial development, are better understood when using a recently proposed six‐part model of pallial divisions. The lizard medial pallium, expressing all genes, includes the medial and dorsomedial cortices, and the majority of the dorsal cortex, except the region of the lateral cortical superposition. The latter is rich in Lhx9 expression, being excluded as a candidate of dorsal or lateral pallia, and may belong to a distinct dorsolateral pallium, which extends from rostral to caudal levels. Thus, the neocortex homolog cannot be found in the classical reptilian dorsal cortex, but perhaps in a small Emx1‐expressing/Lhx9‐negative area at the front of the telencephalon, resembling the avian hyperpallium. The ventral pallium, expressing Lhx9, but not Emx1, gives rise to the dorsal ventricular ridge and appears comparable to the avian nidopallium. We also identified a distinct ventrocaudal pallial sector comparable to the avian arcopallium and to part of the mammalian pallial amygdala. These data open new venues for understanding the organization and evolution of the pallium.

Contribution of Genoarchitecture to Understanding Hippocampal Evolution and Development

“…Unfortunately, data on the expression of early regulatory genes in the developing brain of reptiles are scarce, and the few available results have been interpreted from different viewpoints [for example Suzuki and Hirata, 2014, vs. our interpretation here and in Desfilis et al, 2017]. However, the power of our interpretation resides in that we use a topological reference system for understanding the relative position of the gene expression domains in the neural tube, which is essential for comparative purposes Puelles and Ferrán, 2012;Medina et al, 2013;Nieuwenhuys and Puelles, 2016].…”

“…Our recent data in lizards also provided evidence for the existence of a subdivision, encompassing the Lcs, which appears comparable to a caudal part of the avian dorsolateral pallium [DLP; named temporo-parieto-occipital area by some authors; Reiner et al, 2004;Atoji and Wild, 2005], and to the mammalian LEC [discussed by Desfilis et al, 2017]. Like the mammalian LEC, the lizard Lcs projects to the MC (DG like), and these projections have been suggested to contribute to the reptilian perforant pathway, together with DC2, as mentioned above [López-García et al, 1992].…”

“…Notably, these cortical plates of reptiles that extend laterally above the lateral ventricle highly resemble in position, cytoarchitecture (mostly 3-layered), and molecular profile the hippocampal complex of chicken as it extends laterally above the horn of the lateral ventricle at caudal levels . This comparison reveals a remarkable similarity of the chicken APHcl/CDL with the intermediate sector of the lizard DC (DC2, and more specifically its lateral part), both of which maintain a distinctive strong expression of Lhx9 throughout development [Abellán et al, 2009[Abellán et al, , 2014Desfilis et al, 2017].…”

“…For example, based on Lhx9 expression in the medial pallium of chicken and lizard, the avian APHl/DL appears comparable to the medial part of the reptilian DC2 (DC2-m), as both show moderate expression of this TF during development [Abellán et al, 2014;Desfilis et al, 2017]. Moreover, based on ER81 expression in the medial pallium of chicken and turtle, the avian APHm/DM seems comparable to a medial part of reptilian DC (DC1), as both show a domain rich in expression of this TF during development [Gupta et al, 2012;Suzuki and Hirata, 2014], and both downregulate Lhx9 from intermediate developmental stages [Abellán et al, 2009[Abellán et al, , 2014Desfilis et al, 2017]. If we extrapolate the previous suggestions that chicken APHm+i/DM is comparable to mouse CA1 and chicken APHl/DL resembles the Sub (previous paragraphs), this would mean that the reptilian DC includes subdivisions comparable to either CA1 (DC1) or the Sub (medial part of DC2) ( Table 2 ; Fig.…”

The Secret Caverns of the Dragon’s Brain: Current and Potential Contributions of Lizards to Evolutionary Neuroscience

“…Part of the reason is a lack of data across different amniote lineages, because without comparative data it can be difficult to differentiate a fundamental neural subdivision from a recently derived sub-subdivision unique to a particular group. The study of neuromeric divisions in squamates is critical to overcoming such challenges [Desfilis et al, 2017]. Thus, I collaborated with experts in the neuromeric model to identify and delineate the neuromeric divisions of the dragon brain.…”