Identification of Striatal and Pallidal Regions in the Subpallium of Anamniotes

Abstract

The telencephalic basal ganglia (BG) of amniotes consist of two subdivisions, striatum and pallidum, which share many features, including development, cell types, neurotransmitter organization and hodology. In particular, these two subdivisions during development are defined on the basis of discrete gene expression patterns (genoarchitecture or genoarchitectonics). The characterization of the BG in the subpallium of representatives of the different classes of anamniote vertebrates was first approached in studies dealing with their localization, hodology and main neurochemical characteristics. Thus, it was proposed that an impressive degree of conservation exists across species. New insights can be gained by the comparative analysis of the expression of conserved transcription factors that distinctly define the striatal and pallidal components of the BG in all vertebrates. In addition, the expression of other genes that characterize neighboring regions of the BG is also useful to define the boundaries of each subdivision. Following this approach, we have analyzed the BG in the brain of juvenile representatives of amphibians, lungfishes, holosteans, Polypteriformes and Chondrichthyes. In addition, we briefly review previous data in teleosts and agnathans. The markers used include islet 1 and Dlx as striatal markers, whereas Nkx2.1 is essential for the identification of the pallidum. In turn, Pax6 and in particular Tbr1 are expressed in the pallium. These markers have been systematically analyzed in combination with neuronal markers of specific subpallial territories and cell populations, such as tyrosine hydroxylase, γ-aminobutyric acid, nitric oxide synthase, substance P and enkephalin. The results highlight that many genes share common distribution patterns and are arranged in conserved combinations whose identification has served to define homologies between components of the BG in distant species.

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

“…In particular, the pallidal division, which contains neurons of Nkx2.1 and/or Lhx6 lineage ( table 1 ; fig. 2 ) [Mueller et al, 2008;González and Northcutt, 2009;Mueller and Wullimann, 2009;Quintana-Urzainqui et al, 2012], appears to receive ENK+ and SP+ input from the striatum and also contains LANT6+ cells Northcutt, 1987, 1992; reviewed by González et al, 2014]. Importantly, data on Nkx2.1 expression in lungfishes and cartilaginous fishes have revealed that the pallidal subdivision is smaller (more medially restricted) than previously thought [González and Northcutt, 2009;Quintana-Urzainqui et al, 2012].…”

“…Developmental, neurochemical and connectivity data show that the basal ganglia contain two major subdivisions in all jawed vertebrates studied: an input station called striatum and an output station called pallidum (see reviews by Marín et al [1998]; Reiner et al [1998]; Medina [2009] and González et al [2014]), and recent data in lobe-finned fishes (e.g. lungfishes) [González and Northcutt, 2009], ray-finned fishes (e.g.…”

“…A striatum and a pallidum were identified in lungfishes, ray-finned fishes and cartilaginous fishes based on neurochemical features [Reiner and Northcutt, 1987;Northcutt et al, 1988;Reiner and Northcutt, 1992;Northcutt, 2009], but their delineation has improved thanks to data on the expression of transcription factors during development [Wullimann and Mueller, 2004;Mueller et al, 2008;González and Northcutt, 2009;Mueller and Wullimann, 2009;Quintana-Urzainqui et al, 2012; reviewed by González et al, 2014]. In particular, the pallidal division, which contains neurons of Nkx2.1 and/or Lhx6 lineage ( table 1 ; fig.…”

Subdivisions of the adult zebrafish pallium based on molecular marker analysis

“…This approach has been especially valuable for the telencephalon with its great variability in morphology between vertebrate species and has led to the clarification of the homology within subdivisions of the telencephalon between different vertebrate species, such as the domestic mouse, the chicken and the African clawed frog (e.g. 7– 22 ). For example, the gene expression of Tbr1 and Eomes ( Tbr2 ) has been successfully used to identify the extent of the pallium in tetrapod embryos 9, 21, 23 .…”

Circuits regulating pleasure and happiness: evolution and role in mental disorders

“…Within the anuran forebrain, the striatum (anterior) is continuous with the central and medial amygdala (posterior), and clearly separated from the dorsal/ventral pallidum and the BST and septum (19). An important discovery during the study of the embryological development of anuran basal ganglia was the finding that the BST and part of the septum are also of pallidal instead of striatal origin (23,24). This is interesting because the BST is a suitable structure to execute the limbic component of lamprey GPh.…”