Development and Organization of the Lamprey Telencephalon with Special Reference to the GABAergic System

Abstract

Lampreys, together with hagfishes, represent the sister group of gnathostome vertebrates. There is an increasing interest for comparing the forebrain organization observed in lampreys and gnathostomes to shed light on vertebrate brain evolution. Within the prosencephalon, there is now a general agreement on the major subdivisions of the lamprey diencephalon; however, the organization of the telencephalon, and particularly its pallial subdivisions, is still a matter of controversy. In this study, recent progress on the development and organization of the lamprey telencephalon is reviewed, with particular emphasis on the GABA immunoreactive cell populations trying to understand their putative origin. First, we describe some early general cytoarchitectonic events by searching the classical literature as well as our collection of embryonic and prolarval series of hematoxylin-stained sections. Then, we comment on the cell proliferation activity throughout the larval period, followed by a detailed description of the early events on the development of the telencephalic GABAergic system. In this context, lampreys apparently do not possess the same molecularly distinct subdivisions of the gnathostome basal telencephalon because of the absence of a Nkx2.1-expressing domain in the developing subpallium; a fact that has been related to the absence of a medial ganglionic eminence as well as of its derived nucleus in gnathostomes, the pallidum. Therefore, these data raise interesting questions such as whether or not a different mechanism to specify telencephalic GABAergic neurons exists in lampreys or what are their migration pathways. Finally, we summarize the organization of the adult lamprey telencephalon by analyzing the main proposed conceptions, including the available data on the expression pattern of some developmental regulatory genes which are of importance for building its adult shape.

Development of the γ-amino butyric acid (GABA)-ergic signaling system and its role in larval swimming in sea urchin

“…This was organized further into a GABA-immunoreactive stripe that formed between the two rows of ciliary epithelial cells of the epaulets in eight-arm plutei. Consistent with this finding, the active migration of GABAergic cells during development has been recognized widely (Jelitai and Madarasz, 2005); for example, telencephalon of the sea lamprey, Petromyzon marinus (Pombal et al, 2011), and neocortical projections in mammals (Gilmore and Herrup, 2001). In the sea urchin larvae, the circumoral ciliary band developed extensive accumulation of GABA cells and the larvae acquired sensitivity to GABA-IR deprivation at around the 2d.p.f.…”

Subdivisions of the adult zebrafish subpallium by molecular marker analysis

“…These two genes have not been addressed in the present study. In addition, the pallial-subpallial boundary has been localized in the lamprey, a representative of the jawless vertebrates (agnathans), by expression analysis of the proposed homologs of the dlx genes and GABA expression (Myojin et al, 2001;Murakami et al, 2005;Martinez-de-la-Torre et al, 2011;Pombal et al, 2011). Orthology between agnathan and jawed vertebrate genes is difficult to infer due to the unclear timing of the two vertebrate genome duplications with respect to the divergence of agnathans and gnathostomes, differential evolutionary rates, and gene losses in agnathan and gnathostome genomes Kuraku, 2008;Kuraku et al, 2009), and the lack of a finished lamprey genome assembly.…”

Integrative Neuro-Endocrine Pathways in the Control of Reproduction in Lamprey: A Brief Review

“…Aside from the central role of the GnRH however, much less is understood from reproductive neurobiology of lamprey and of agnathans in general. There is an important body of information available on chemical neuroanatomy of lamprey brain, collected more recently through the efforts of research groups like Pombal in Spain (90) or Grillner in Sweden (91) among others. These efforts contributed to a deeper understanding of the evolutionary developmental origins of the vertebrate brain and also they allowed the lamprey locomotor system to become one of the best understood in vertebrates.…”