Young adult born neurons enhance hippocampal dependent performance via influences on bilateral networks

Abstract

Adult neurogenesis supports performance in many hippocampal dependent tasks. Considering the small number of adult-born neurons generated at any given time, it is surprising that this sparse population of cells can substantially influence behavior. Recent studies have demonstrated that heightened excitability and plasticity may be critical for the contribution of young adult-born cells for certain tasks. What is not well understood is how these unique biophysical and synaptic properties may translate to networks that support behavioral function. Here we employed a location discrimination task in mice while using optogenetics to transiently silence adult-born neurons at different ages. We discovered that adult-born neurons promote location discrimination during early stages of development but only if they undergo maturation during task acquisition. Silencing of young adult-born neurons also produced changes extending to the contralateral hippocampus, detectable by both electrophysiology and fMRI measurements, suggesting young neurons may modulate location discrimination through influences on bilateral hippocampal networks.

Article and author information

Author details

  1. Jia-Min Zhuo

    Biomedical Engineering, Boston University, Boston, United States
    For correspondence
    jmzhuo2002@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Hua-an Tseng

    Biomedical Engineering Department, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Mitul Desai

    Department of Bioengineering, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Mark E Bucklin

    Biomedical Engineering Department, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ali I Mohammed

    Biomedical Engineering Department, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Nick TM Robinson

    Department of Psychology, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Edward S Boyden

    Department of Bioengineering, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Lara M Rangel

    Department of Psychology, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Alan P Jasanoff

    Department of Bioengineering, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Howard J Gritton

    Biomedical Engineering Department, Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3194-3258
  11. Xue Han

    Biomedical Engineering Department, Boston University, Boston, United States
    For correspondence
    xuehan@bu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3896-4609

Funding

NIH Office of the Director (1DP2NS082126)

  • Xue Han

National Institute of Mental Health (5R00MH085944, 1R21MH109941)

  • Xue Han

NIH Office of the Director (R01-DA028299)

  • Alan P Jasanoff

Defense Advanced Research Projects Agency (W911NF-10-0059)

  • Alan P Jasanoff

Pew Charitable Trusts

  • Xue Han

American Federation for Aging Research

  • Jia-Min Zhuo

Alfred P. Sloan Foundation

  • Xue Han

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

Reviewing Editor

  1. Marlene Bartos, Albert-Ludwigs-Universität Freiburg, Germany

Ethics

Animal experimentation: All procedures involving animals were in accordance with the National Institutes of Health Guide for the care and use of Laboratory Animals, and approved by the Boston University and Massachusetts Institute of Technology Animal Care and Use Committee (protocol #'s: BU: 15-010; MIT: 1115-111-18).

Version history

  1. Received: October 15, 2016
  2. Accepted: November 16, 2016
  3. Accepted Manuscript published: December 3, 2016 (version 1)
  4. Version of Record published: December 14, 2016 (version 2)

Copyright

© 2016, Zhuo 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. Jia-Min Zhuo
  2. Hua-an Tseng
  3. Mitul Desai
  4. Mark E Bucklin
  5. Ali I Mohammed
  6. Nick TM Robinson
  7. Edward S Boyden
  8. Lara M Rangel
  9. Alan P Jasanoff
  10. Howard J Gritton
  11. Xue Han
(2016)
Young adult born neurons enhance hippocampal dependent performance via influences on bilateral networks
eLife 5:e22429.
https://doi.org/10.7554/eLife.22429

Share this article

https://doi.org/10.7554/eLife.22429

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