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Locomotion-induced ocular motor behavior in larval Xenopus is developmentally tuned by visuo-vestibular reflexes

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  • Julien Bacqué-Cazenave

    (Université de Bordeaux, CNRS UMR 5287, Institut de Neurosciences Cognitives et Intégratives d’Aquitaine
    Normandie Univ, Unicaen, CNRS, EthoS
    Univ Rennes, CNRS, EthoS (Éthologie animale et humaine)—UMR 6552)

  • Gilles Courtand

    (Université de Bordeaux, CNRS UMR 5287, Institut de Neurosciences Cognitives et Intégratives d’Aquitaine)

  • Mathieu Beraneck

    (Université de Paris, CNRS UMR 8002, Integrative Neuroscience and Cognition Center)

  • Hans Straka

    (Faculty of Biology, Ludwig-Maximilians-University Munich)

  • Denis Combes

    (Université de Bordeaux, CNRS UMR 5287, Institut de Neurosciences Cognitives et Intégratives d’Aquitaine)

  • François M. Lambert

    (Université de Bordeaux, CNRS UMR 5287, Institut de Neurosciences Cognitives et Intégratives d’Aquitaine)

Abstract

Locomotion in vertebrates is accompanied by retinal image-stabilizing eye movements that derive from sensory-motor transformations and predictive locomotor efference copies. During development, concurrent maturation of locomotor and ocular motor proficiency depends on the structural and neuronal capacity of the motion detection systems, the propulsive elements and the computational capability for signal integration. In developing Xenopus larvae, we demonstrate an interactive plasticity of predictive locomotor efference copies and multi-sensory motion signals to constantly elicit dynamically adequate eye movements during swimming. During ontogeny, the neuronal integration of vestibulo- and spino-ocular reflex components progressively alters as locomotion parameters change. In young larvae, spino-ocular motor coupling attenuates concurrent angular vestibulo-ocular reflexes, while older larvae express eye movements that derive from a combination of the two components. This integrative switch depends on the locomotor pattern generator frequency, represents a stage-independent gating mechanism, and appears during ontogeny when the swim frequency naturally declines with larval age.

Suggested Citation

  • Julien Bacqué-Cazenave & Gilles Courtand & Mathieu Beraneck & Hans Straka & Denis Combes & François M. Lambert, 2022. "Locomotion-induced ocular motor behavior in larval Xenopus is developmentally tuned by visuo-vestibular reflexes," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-30636-6
    DOI: 10.1038/s41467-022-30636-6
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    References listed on IDEAS

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    1. Boris P. Chagnaud & Roberto Banchi & John Simmers & Hans Straka, 2015. "Spinal corollary discharge modulates motion sensing during vertebrate locomotion," Nature Communications, Nature, vol. 6(1), pages 1-14, November.
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