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Delayed and asynchronous ganglionic maturation during cephalopod neurogenesis as evidenced by Sof-elav1 expression in embryos of Sepia officinalis (Mollusca, Cephalopoda)

Authors

  • Auxane Buresi,

    Corresponding author
    1. Muséum National d'Histoire Naturelle (MNHN), DMPA, UMR Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), MNHN CNRS 7208, IRD 207, UPMC, 75005 Paris, France
    2. Université Paris Pierre et Marie Curie, Paris 6, Paris, France
    • 55 rue Buffon, CP51 75005 Paris, France
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  • Ester Canali,

    1. Stazione Zoologica Anton Dohrn, Villa Comunale, 80121 Napoli, Italy
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  • Laure Bonnaud,

    1. Muséum National d'Histoire Naturelle (MNHN), DMPA, UMR Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), MNHN CNRS 7208, IRD 207, UPMC, 75005 Paris, France
    2. Université Paris Diderot, Sorbonne Paris Cité, Paris, France
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  • Sébastien Baratte

    1. Muséum National d'Histoire Naturelle (MNHN), DMPA, UMR Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), MNHN CNRS 7208, IRD 207, UPMC, 75005 Paris, France
    2. Université Paris Sorbonne, Paris 4, Paris France
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Abstract

Among the Lophotrochozoa, centralization of the nervous system reaches an exceptional level of complexity in cephalopods, where the typical molluscan ganglia become highly developed and fuse into hierarchized lobes. It is known that ganglionic primordia initially emerge early and simultaneously during cephalopod embryogenesis but no data exist on the process of neuron differentiation in this group. We searched for members of the elav/hu family in the cuttlefish Sepia officinalis, since they are one of the first genetic markers of postmitotic neural cells. Two paralogs were identified and the expression of the most neural-specific gene, Sof-elav1, was characterized during embryogenesis. Sof-elav1 is expressed in all ganglia at one time of development, which provides the first genetic map of neurogenesis in a cephalopod. Our results unexpectedly revealed that Sof-elav1 expression is not similar and not coordinated in all the prospective ganglia. Both palliovisceral ganglia show extensive Sof-elav1 expression soon after emergence, showing that most of their cells differentiate into neurons at an early stage. On the contrary, other ganglia, and especially both cerebral ganglia that contribute to the main parts of the brain learning centers, show a late extensive Sof-elav1 expression. These delayed expressions in ganglia suggest that most ganglionic cells retain their proliferative capacities and postpone differentiation. In other molluscs, where a larval nervous system predates the development of the definitive adult nervous system, cerebral ganglia are among the first to mature. Thus, such a difference may constitute a cue in understanding the peculiar brain evolution in cephalopods. J. Comp. Neurol. 521:1482–1496, 2013. © 2012 Wiley Periodicals, Inc.

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