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

Author:

Bloch Solal1,Hagio Hanako23ORCID,Thomas Manon1,Heuzé Aurélie1,Hermel Jean-Michel1ORCID,Lasserre Elodie1,Colin Ingrid1,Saka Kimiko4ORCID,Affaticati Pierre5,Jenett Arnim5,Kawakami Koichi46ORCID,Yamamoto Naoyuki2,Yamamoto Kei1ORCID

Affiliation:

1. Paris-Saclay Institute of Neuroscience (Neuro-PSI), Université Paris-Saclay, CNRS, Gif-sur-Yvette, France

2. Laboratory of Fish Biology, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan

3. Institute for Advanced Research, Nagoya University, Nagoya, Japan

4. Laboratory of Molecular and Developmental Biology, National Institute of Genetics, Mishima, Japan

5. TEFOR Paris-Saclay, CNRS UMS2010, INRA UMS1451, Université Paris-Saclay, Gif-sur-Yvette, France

6. Department of Genetics, SOKENDAI (The Graduate University for Advanced Studies), Mishima, Japan

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.

Funder

Agence Nationale de la Recherche

Fondation pour la Recherche Médicale

Japan Society for the Promotion of Science

Japan Agency for Medical Research and Development

National Institut of Genetics and NBRP

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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