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Perturbed Wnt signaling leads to neuronal migration delay, altered interhemispheric connections and impaired social behavior

Author

Listed:
  • Riccardo Bocchi

    (University of Geneva Medical School)

  • Kristof Egervari

    (University of Geneva Medical School)

  • Laura Carol-Perdiguer

    (University of Geneva Medical School)

  • Beatrice Viale

    (University of Geneva Medical School)

  • Charles Quairiaux

    (University of Geneva Medical School)

  • Mathias Roo

    (University of Geneva Medical School)

  • Michael Boitard

    (University of Geneva Medical School)

  • Suzanne Oskouie

    (University of Geneva Medical School)

  • Patrick Salmon

    (University of Geneva Medical School)

  • Jozsef Z. Kiss

    (University of Geneva Medical School)

Abstract

Perturbed neuronal migration and circuit development have been implicated in the pathogenesis of neurodevelopmental diseases; however, the direct steps linking these developmental errors to behavior alterations remain unknown. Here we demonstrate that Wnt/C-Kit signaling is a key regulator of glia-guided radial migration in rat somatosensory cortex. Transient downregulation of Wnt signaling in migrating, callosal projection neurons results in delayed positioning in layer 2/3. Delayed neurons display reduced neuronal activity with impaired afferent connectivity causing permanent deficit in callosal projections. Animals with these defects exhibit altered somatosensory function with reduced social interactions and repetitive movements. Restoring normal migration by overexpressing the Wnt-downstream effector C-Kit or selective chemogenetic activation of callosal projection neurons during a critical postnatal period prevents abnormal interhemispheric connections as well as behavioral alterations. Our findings identify a link between defective canonical Wnt signaling, delayed neuronal migration, deficient interhemispheric connectivity and abnormal social behavior analogous to autistic characteristics in humans.

Suggested Citation

  • Riccardo Bocchi & Kristof Egervari & Laura Carol-Perdiguer & Beatrice Viale & Charles Quairiaux & Mathias Roo & Michael Boitard & Suzanne Oskouie & Patrick Salmon & Jozsef Z. Kiss, 2017. "Perturbed Wnt signaling leads to neuronal migration delay, altered interhemispheric connections and impaired social behavior," Nature Communications, Nature, vol. 8(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_s41467-017-01046-w
    DOI: 10.1038/s41467-017-01046-w
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    Cited by:

    1. Christelle Glangetas & Adriane Guillaumin & Elodie Ladevèze & Anaelle Braine & Manon Gauthier & Léa Bonamy & Evelyne Doudnikoff & Thibault Dhellemmes & Marc Landry & Erwan Bézard & Stephanie Caille & , 2024. "A population of Insula neurons encodes for social preference only after acute social isolation in mice," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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