Non-thalamic origin of zebrafish sensory nuclei implies convergent evolution of visual pathways in amniotes and teleosts.

Solal Bloch,Ingrid Colin,Hanako Hagio,Pierre Affaticati,Kimiko Saka,Elodie Lasserre,Koichi Kawakami,Naoyuki Yamamoto,Aurélie Heuzé,Jean-Michel Hermel,Manon Thomas,Kei Yamamoto,Arnim Jenett

doi:10.7554/elife.54945

Abstract

Ascending visual projections similar to the mammalian thalamocortical pathway are found in a wide range of vertebrate species, but their homology is debated. To get better insights into their evolutionary origin, we examined the developmental origin of a thalamic-like sensory structure of teleosts, the preglomerular complex (PG), focusing on the visual projection neurons. Similarly to the tectofugal thalamic nuclei in amniotes, the lateral nucleus of PG receives tectal information and projects to the pallium. However, our cell lineage study in zebrafish reveals that the majority of PG cells are derived from the midbrain, unlike the amniote thalamus. We also demonstrate that the PG projection neurons develop gradually until late juvenile stages. Our data suggest that teleost PG, as a whole, is not homologous to the amniote thalamus. Thus, the thalamocortical-like projections evolved from a non-forebrain cell population, which indicates a surprising degree of variation in the vertebrate sensory systems.

Highlights

It is accepted that all vertebrate brains possess three major divisions: the forebrain, midbrain, and hindbrain
We identified a Gal4-expressing transgenic fish line, Tg(gSAGFF279A) crossed with Tg(UAS: GFP), which had GFP-positive (GFP+) cells projecting to a part of the pallium (Supplementary file 1)
In the Tg(279A-GFP), abundant GFP+ fibers are present in dorsal telencephalic area (Dl) (Figure 2A), and GFP+ cell bodies are found in a part of preglomerular complex (PG) (Figure 2B). 3D reconstruction of confocal images of the entire brain allowed us to follow the projection from the PG to the pallium (Figure 2C,D and Video 1)

Summary

Introduction

It is accepted that all vertebrate brains possess three major divisions: the forebrain (prosencephalon), midbrain (mesencephalon), and hindbrain (rhombencephalon). It is a fundamental question to evaluate to what extent the functional connectivity is conserved among different vertebrate groups (Güntürkün, 2005; Yamamoto and Bloch, 2017; Striedter and Northcutt, 2020). This issue has been difficult to address, because connectivity patterns are often similar across vertebrate groups. There is no consensus on the regional homology of the related brain structures across species This is illustrated by the still ongoing discussions about the evolutionary history of the sensory ascending pathways and thalamorecipient pallial areas in amniotes (a group containing mammals and birds). Homology of the target pallial areas has been under debate (Karten and Shimizu, 1989; Bruce and Neary, 1995; Striedter, 1997; Puelles et al, 2000; Butler et al, 2011; Dugas-Ford et al, 2012)

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