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Non-thalamic origin of zebrafish sensory relay nucleus: convergent evolution of visual pathways in amniotes and teleosts

Solal Bloch, Hanako Hagio, Manon Thomas, Aurélie Heuzé, Jean-Michel Hermel, Elodie Lasserre, Ingrid Colin, Kimiko Saka, Pierre Affaticati, Arnim Jenett, Koichi Kawakami, Naoyuki Yamamoto, View ORCID ProfileKei Yamamoto
doi: https://doi.org/10.1101/2020.05.16.099010
Solal Bloch
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Université Paris-Saclay, CNRS, 91190 Gif-sur-Yvette, France
7Department of Neuroscience, Charleston Alcohol Research Center, Medical University of South Carolina, Charleston, South Carolina 29425, USA
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Hanako Hagio
2Laboratory of Fish Biology, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan
3Institute for Advanced Research, Nagoya University, Nagoya 464-8601, Japan
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Manon Thomas
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Université Paris-Saclay, CNRS, 91190 Gif-sur-Yvette, France
8Plateau de phénotypage TEFOR, LPGP-INRA UR1037, 35042 Rennes, France
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Aurélie Heuzé
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Université Paris-Saclay, CNRS, 91190 Gif-sur-Yvette, France
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Jean-Michel Hermel
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Université Paris-Saclay, CNRS, 91190 Gif-sur-Yvette, France
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Elodie Lasserre
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Université Paris-Saclay, CNRS, 91190 Gif-sur-Yvette, France
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Ingrid Colin
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Université Paris-Saclay, CNRS, 91190 Gif-sur-Yvette, France
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Kimiko Saka
4Laboratory of Molecular and Developmental Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan
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Pierre Affaticati
6TEFOR Paris-Saclay, CNRS UMS2010, INRA UMS1451, Université Paris-Saclay, 91190 Gif-sur-Yvette, France
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Arnim Jenett
6TEFOR Paris-Saclay, CNRS UMS2010, INRA UMS1451, Université Paris-Saclay, 91190 Gif-sur-Yvette, France
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Koichi Kawakami
4Laboratory of Molecular and Developmental Biology, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan
5Department of Genetics, SOKENDAI (The Graduate University for Advanced Studies), Mishima, Shizuoka 411-8540, Japan
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Naoyuki Yamamoto
2Laboratory of Fish Biology, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan
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Kei Yamamoto
1Paris-Saclay Institute of Neuroscience (Neuro-PSI), Université Paris-Saclay, CNRS, 91190 Gif-sur-Yvette, France
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  • ORCID record for Kei Yamamoto
  • For correspondence: kei.yamamoto@cnrs.fr
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Abstract

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

Competing Interest Statement

The authors have declared no competing interest.

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Non-thalamic origin of zebrafish sensory relay nucleus: convergent evolution of visual pathways in amniotes and teleosts
Solal Bloch, Hanako Hagio, Manon Thomas, Aurélie Heuzé, Jean-Michel Hermel, Elodie Lasserre, Ingrid Colin, Kimiko Saka, Pierre Affaticati, Arnim Jenett, Koichi Kawakami, Naoyuki Yamamoto, Kei Yamamoto
bioRxiv 2020.05.16.099010; doi: https://doi.org/10.1101/2020.05.16.099010
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Non-thalamic origin of zebrafish sensory relay nucleus: convergent evolution of visual pathways in amniotes and teleosts
Solal Bloch, Hanako Hagio, Manon Thomas, Aurélie Heuzé, Jean-Michel Hermel, Elodie Lasserre, Ingrid Colin, Kimiko Saka, Pierre Affaticati, Arnim Jenett, Koichi Kawakami, Naoyuki Yamamoto, Kei Yamamoto
bioRxiv 2020.05.16.099010; doi: https://doi.org/10.1101/2020.05.16.099010

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