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Dipolar extracellular potentials generated by axonal projections

  1. Thomas McColgan  Is a corresponding author
  2. Ji Liu
  3. Paula Tuulia Kuokkanen
  4. Catherine Emily Carr
  5. Hermann Wagner
  6. Richard Kempter  Is a corresponding author
  1. Institute of Theoretical Biology, Humboldt-Universität zu Berlin, Germany
  2. University of Maryland, United States
  3. RWTH Aachen, Germany
Research Article
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Cite this article as: eLife 2017;6:e26106 doi: 10.7554/eLife.26106

Abstract

Extracellular field potentials (EFPs) are an important source of information in neuroscience, but their physiological basis is in many cases still a matter of debate. Axonal sources are typically discounted in modeling and data analysis because their contributions are assumed to be negligible. Here, we established experimentally and theoretically that contributions of axons to EFPs can be significant. Modeling action potentials propagating along axons, we showed that EFPs were prominent in the presence of terminal zones where axons branch and terminate in close succession, as found in many brain regions. Our models predicted a dipolar far field and a polarity reversal at the center of the terminal zone. We confirmed these predictions using EFPs from the barn owl auditory brainstem where we recorded in nucleus laminaris using a multielectrode array. These results demonstrate that axonal terminal zones can produce EFPs with considerable amplitude and spatial reach.

Article and author information

Author details

  1. Thomas McColgan

    Department of Biology, Institute of Theoretical Biology, Humboldt-Universität zu Berlin, Berlin, Germany
    For correspondence
    thomas.mccolgan@gmail.com
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0027-0580
  2. Ji Liu

    Department of Biology, University of Maryland, College Park, United States
    Competing interests
    No competing interests declared.
  3. Paula Tuulia Kuokkanen

    Department of Biology, Institute of Theoretical Biology, Humboldt-Universität zu Berlin, Berlin, Germany
    Competing interests
    No competing interests declared.
  4. Catherine Emily Carr

    Department of Biology, University of Maryland, College Park, United States
    Competing interests
    Catherine Emily Carr, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5698-6014
  5. Hermann Wagner

    Institute for Biology II, RWTH Aachen, Aachen, Germany
    Competing interests
    No competing interests declared.
  6. Richard Kempter

    Department of Biology, Institute of Theoretical Biology, Humboldt-Universität zu Berlin, Berlin, Germany
    For correspondence
    r.kempter@biologie.hu-berlin.de
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5344-2983

Funding

National Institute on Deafness and Other Communication Disorders (DC-00436)

  • Catherine Emily Carr

German Ministry for Education and Research (01GQ1001A)

  • Richard Kempter

Collaborative Research in Computational Neuroscience Program (01GQ1505A)

  • Richard Kempter

National Science Foundation (1516357)

  • Catherine Emily Carr

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

Ethics

Animal experimentation: This study was performed in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols R-13-14 and R-16-11 of the University of Maryland. All experiments were non-recovery, with surgery performed under urethane anesthesia."

Reviewing Editor

  1. Mark CW van Rossum, University of Edinburgh, United Kingdom

Publication history

  1. Received: March 6, 2017
  2. Accepted: September 1, 2017
  3. Accepted Manuscript published: September 5, 2017 (version 1)
  4. Version of Record published: September 27, 2017 (version 2)

Copyright

© 2017, McColgan 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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