Massive normalization of olfactory bulb output in mice with a 'monoclonal nose'

  1. Benjamin Roland
  2. Rebecca Jordan
  3. Dara L Sosulski
  4. Assunta Diodato
  5. Izumi Fukunaga
  6. Ian Wickersham
  7. Kevin M Franks
  8. Andreas T Schaefer
  9. Alexander Fleischmann  Is a corresponding author
  1. Collège de France, France
  2. The Francis Crick Institute, United Kingdom
  3. University College London, United Kingdom
  4. Massachusetts Institute of Technology, United States
  5. Duke University, United States

Abstract

Perturbations in neural circuits can provide mechanistic understanding of the neural correlates of behavior. In M71 transgenic mice with a 'monoclonal nose', glomerular input patterns in the olfactory bulb are massively perturbed and olfactory behaviors are altered. To gain insights into how olfactory circuits can process such degraded inputs we characterized odor-evoked responses of olfactory bulb mitral cells and interneurons. Surprisingly, calcium imaging experiments reveal that mitral cell responses in M71 transgenic mice are largely normal, highlighting a remarkable capacity of olfactory circuits to normalize sensory input. In vivo whole cell recordings suggest that feedforward inhibition from olfactory bulb periglomerular cells can mediate this signal normalization. Together, our results identify inhibitory circuits in the olfactory bulb as a mechanistic basis for many of the behavioral phenotypes of mice with a 'monoclonal nose' and highlight how substantially degraded odor input can be transformed to yield meaningful olfactory bulb output.

Article and author information

Author details

  1. Benjamin Roland

    Center for Interdisciplinary Research in Biology, Collège de France, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Rebecca Jordan

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Dara L Sosulski

    Wolfson Institute for Biomedical Research, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Assunta Diodato

    Center for Interdisciplinary Research in Biology, Collège de France, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Izumi Fukunaga

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Ian Wickersham

    MIT Genetic Neuroengineering Group, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Kevin M Franks

    Department of Neurobiology, Duke University, Durham, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Andreas T Schaefer

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Alexander Fleischmann

    Center for Interdisciplinary Research in Biology, Collège de France, Paris, France
    For correspondence
    alexander.fleischmann@college-de-france.fr
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All experiments were performed in accordance with approved institutional animal care and use committee protocols of Columbia University (#AC-AAAH9255), and in accordance with the INSERM Animal Care and Use Committee guidelines (#B750512/00615.02), the German Animal Welfare Act, and the UK Home Office and the Animals and Scientific Procedures Act (#PPL 70/7827).

Reviewing Editor

  1. Upinder S Bhalla, National Centre for Biological Sciences, India

Publication history

  1. Received: March 23, 2016
  2. Accepted: May 12, 2016
  3. Accepted Manuscript published: May 13, 2016 (version 1)
  4. Version of Record published: June 23, 2016 (version 2)
  5. Version of Record updated: June 29, 2016 (version 3)

Copyright

© 2016, Roland 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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  1. Benjamin Roland
  2. Rebecca Jordan
  3. Dara L Sosulski
  4. Assunta Diodato
  5. Izumi Fukunaga
  6. Ian Wickersham
  7. Kevin M Franks
  8. Andreas T Schaefer
  9. Alexander Fleischmann
(2016)
Massive normalization of olfactory bulb output in mice with a 'monoclonal nose'
eLife 5:e16335.
https://doi.org/10.7554/eLife.16335
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