1. Developmental Biology
  2. Neuroscience
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A mutant with bilateral whisker to barrel inputs unveils somatosensory mapping rules in the cerebral cortex

  1. Nicolas Renier  Is a corresponding author
  2. Chloe Dominici
  3. Reha S Erzurumlu
  4. Claudius F Kratochwil
  5. Filippo M Rijli
  6. Patricia Gaspar
  7. Alain Chédotal  Is a corresponding author
  1. Hôpital de la Pitié-Salpétrière, France
  2. Sorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, France
  3. University of Maryland School of Medicine, United States
  4. University of Konstanz, Germany
  5. Friedrich Miescher Institute for Biomedical Research, Switzerland
  6. INSERM, U839, Institut du Fer à Moulin, France
Research Article
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Cite this article as: eLife 2017;6:e23494 doi: 10.7554/eLife.23494

Abstract

In mammals, tactile information is mapped topographically onto the contralateral side of the brain in the primary somatosensory cortex (S1). Here we describe that in Robo3 mouse mutants a sizeable fraction of the trigemino-thalamic inputs project ipsilaterally rather than contralaterally. The resulting mixture of crossed and uncrossed sensory inputs creates bilateral whisker maps in the thalamus and cortex. Surprisingly, these maps are segregated resulting in a duplication of whisker representations and a doubling of the number of barrels without changes of the S1 size. Sensory deprivation shows competitive interactions between the ipsi/contralateral whisker maps. This study reveals that the somatosensory system can form a somatotopic map to integrate bilateral sensory inputs but organizes the maps in a different way than in the visual, or auditory systems. Therefore, while the molecular pre-patterning constrains their orientation and position, the preservation of the continuity of inputs defines the layout of the somatosensory maps.

Article and author information

Author details

  1. Nicolas Renier

    ICM - Brain and Spine Institute, Hôpital de la Pitié-Salpétrière, Paris, France
    For correspondence
    nicolas.renier@mail.rockefeller.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Chloe Dominici

    Institut de la Vision, Sorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Reha S Erzurumlu

    Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Claudius F Kratochwil

    Chair in Zoology and Evolutionary Biology, Department of Biology, University of Konstanz, Konstanz, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5646-3114
  5. Filippo M Rijli

    Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0515-0182
  6. Patricia Gaspar

    INSERM, U839, Institut du Fer à Moulin, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Alain Chédotal

    Institut de la Vision, Sorbonne Universités, UPMC Univ Paris 06, INSERM, CNRS, Paris, France
    For correspondence
    alain.chedotal@inserm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7577-3794

Funding

Agence Nationale de la Recherche (ANR-08-MNP-030,ANR-08,MNP-032,ANR-14-CE13-0004-01,ANR-10-LABX-65)

  • Filippo M Rijli
  • Patricia Gaspar
  • Alain Chédotal

Fondation pour la Recherche Médicale (DEQ20120323700)

  • Alain Chédotal

National Institute of Neurological Disorders and Stroke (RO1 NS039050)

  • Reha S Erzurumlu

swiss national science foundation (CRSI33_127440)

  • Filippo M Rijli

Association Française contre les Myopathies

  • Nicolas Renier

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All animal procedures were carried out in accordance to institutional guidelines and approved by the UPMC University ethic committee (ComitÃ{copyright, serif} Charles Darwin, authorization # 03787.02). All surgery was performed under ketamine/xylazine anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Carol A Mason, Columbia University, United States

Publication history

  1. Received: November 21, 2016
  2. Accepted: March 27, 2017
  3. Accepted Manuscript published: March 28, 2017 (version 1)
  4. Accepted Manuscript updated: April 3, 2017 (version 2)
  5. Version of Record published: April 25, 2017 (version 3)

Copyright

© 2017, Renier et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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