Tangential migratory pathways of subpallial origin in the embryonic telencephalon of sharks: evolutionary implications

Abstract

Tangential neuronal migration occurs along different axes from the axis demarcated by radial glia and it is thought to have evolved as a mechanism to increase the diversity of cell types in brain areas, which in turn resulted in increased complexity of functional networks. In the telencephalon of amniotes, different embryonic tangential pathways have been characterized. However, little is known about the exact routes of migrations in basal vertebrates. Cartilaginous fishes occupy a key phylogenetic position to assess the ancestral condition of vertebrate brain organization. In order to identify putative subpallial-derived tangential migratory pathways in the telencephalon of sharks, we performed a detailed analysis of the distribution pattern of GAD and Dlx2, two reliable markers of tangentially migrating interneurons of subpallial origin in the developing forebrain. We propose the existence of five tangential routes directed toward different telencephalic regions. We conclude that four of the five routes might have emerged in the common ancestor of jawed vertebrates. We have paid special attention to the characterization of the proposed migratory pathway directed towards the olfactory bulbs. Our results suggest that it may be equivalent to the "rostral migratory stream" of mammals and led us to propose a hypothesis about its evolution. The analysis of the final destinations of two other streams allowed us to identify the putative dorsal and medial pallium of sharks, the regions from which the neocortex and hippocampus might have, respectively, evolved. Derived features were also reported and served to explain some distinctive traits in the morphology of the telencephalon of cartilaginous fishes.

The Shark Alar Hypothalamus: Molecular Characterization of Prosomeric Subdivisions and Evolutionary Trends

“…As previously reported, they are especially abundant in the PPa area, rostral diencephalon and pallium (Ferreiro-Galve et al, 2008; Rodríguez-Moldes, 2009; Quintana-Urzainqui et al, 2015). …”

“…From stage 31 this pattern is maintained in the alar hypothalamus, and the changes observed in the telencephalon were already reported (see Quintana-Urzainqui et al, 2015). …”

“…We applied ISH for ScOtp (Santos-Durán et al, 2015), ScDlx2 (Quintana-Urzainqui et al, 2012, 2015; Compagnucci et al, 2013; Debiais-Thibaud et al, 2013; Santos-Durán et al, 2015), ScDlx5 (Compagnucci et al, 2013; Debiais-Thibaud et al, 2013; Santos-Durán et al, 2015), ScLhx9 (Pose-Méndez et al, 2015; Quintana-Urzainqui et al, 2015), ScLhx5, ScNkx2 (Quintana-Urzainqui et al, 2012, 2015; Santos-Durán et al, 2015), ScNkx2.8, ScTbr1 (Quintana-Urzainqui et al, 2015; Santos-Durán et al, 2015), and ScNeurog2 genes. These probes were selected from a collection of S. canicula embryonic cDNA library (mixed stages S9–S22), constructed in pSPORT1, and submitted to high throughput EST sequencing.…”

A Developmental Study of the Cerebellar Nucleus in the Catshark, a Basal Gnathostome

“…Tbr1 is best known for its role in specifying glutamatergic pyramidal neurons in the rodent cerebral cortex [Hodge et al, 2012]. Moreover, the pattern of ScTbr1 expression was complementary to that of ScDlx2 (a marker of GABAergic subpallial cells) in the telencephalon of S. canicula [Quintana-Urzainqui et al, 2015], which is consistent with its involvement in differentiation of pallial glutamatergic cells. The codistribution of ScLhx9 and ScTbr1 expressions with Pax6-ir cells in nonGABAergic cells of the MZ of S. canicula also suggests the possibility that these transcription factors are coexpressed in differentiating glutamatergic cells.…”

“…In situ hybridization was applied on sections for the genes ScTbr1 [Quintana-Urzainqui et al, 2015;Santos-Durán et al, 2015], ScEn2 [Pose-Méndez et al, 2016a, b], ScLhx9 [QuintanaUrzainqui et al, 2015;Pose-Méndez et al, 2016a], and ScLhx5. These probes were selected from a collection of S. canicula embryonic cDNA library (mixed stages, S9 to S22) submitted to highthroughput EST sequencing (coordinated by S. Mazan).…”