1. Developmental Biology
  2. Neuroscience
Download icon

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
  • Cited 14
  • Views 2,598
  • Annotations
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@icm-institute.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2642-4402
  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.

Metrics

  • 2,598
    Page views
  • 671
    Downloads
  • 14
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Developmental Biology
    2. Stem Cells and Regenerative Medicine
    Alessandro Bonfini et al.
    Research Article

    The gut is the primary interface between an animal and food, but how it adapts to qualitative dietary variation is poorly defined. We find that the Drosophila midgut plastically resizes following changes in dietary composition. A panel of nutrients collectively promote gut growth, which sugar opposes. Diet influences absolute and relative levels of enterocyte loss and stem cell proliferation, which together determine cell numbers. Diet also influences enterocyte size. A high sugar diet inhibits translation and uncouples ISC proliferation from expression of niche-derived signals but, surprisingly, rescuing these effects genetically was not sufficient to modify diet's impact on midgut size. However, when stem cell proliferation was deficient, diet's impact on enterocyte size was enhanced, and reducing enterocyte-autonomous TOR signaling was sufficient to attenuate diet-dependent midgut resizing. These data clarify the complex relationships between nutrition, epithelial dynamics, and cell size, and reveal a new mode of plastic, diet-dependent organ resizing.

    1. Developmental Biology
    2. Physics of Living Systems
    Yonghyun Song, Changbong Hyeon
    Research Article Updated

    Spatial boundaries formed during animal development originate from the pre-patterning of tissues by signaling molecules, called morphogens. The accuracy of boundary location is limited by the fluctuations of morphogen concentration that thresholds the expression level of target gene. Producing more morphogen molecules, which gives rise to smaller relative fluctuations, would better serve to shape more precise target boundaries; however, it incurs more thermodynamic cost. In the classical diffusion-depletion model of morphogen profile formation, the morphogen molecules synthesized from a local source display an exponentially decaying concentration profile with a characteristic length λ. Our theory suggests that in order to attain a precise profile with the minimal cost, λ should be roughly half the distance to the target boundary position from the source. Remarkably, we find that the profiles of morphogens that pattern the Drosophila embryo and wing imaginal disk are formed with nearly optimal λ. Our finding underscores the cost-effectiveness of precise morphogen profile formation in Drosophila development.