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Generalization of learned responses in the mormyrid electrosensory lobe

  1. Conor Dempsey
  2. L F Abbott
  3. Nathaniel B Sawtell  Is a corresponding author
  1. Columbia University, United States
Research Article
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Cite this article as: eLife 2019;8:e44032 doi: 10.7554/eLife.44032

Abstract

Appropriate generalization of learned responses to new situations is vital for adaptive behavior. We provide a circuit-level account of generalization in the electrosensory lobe (ELL) of weakly electric mormyrid fish. Much is already known in this system about a form of learning in which motor corollary discharge signals cancel responses to the uninformative input evoked by the fish's own electric pulses. However, for this cancellation to be useful under natural circumstances, it must generalize accurately across behavioral regimes, specifically different electric pulse rates. We show that such generalization indeed occurs in ELL neurons, and develop a circuit-level model explaining how this may be achieved. The mechanism involves regularized synaptic plasticity and an approximate matching of the temporal dynamics of motor corollary discharge and electrosensory inputs. Recordings of motor corollary discharge signals in mossy fibers and granule cells provide direct evidence for such matching.

Article and author information

Author details

  1. Conor Dempsey

    Department of Neuroscience, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. L F Abbott

    Department of Neuroscience, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Nathaniel B Sawtell

    Department of Neuroscience, Columbia University, New York, United States
    For correspondence
    ns2635@columbia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1859-8026

Funding

National Science Foundation (1025849)

  • L F Abbott
  • Nathaniel B Sawtell

National Institute of Neurological Disorders and Stroke (NS075023)

  • Nathaniel B Sawtell

Irma T. Hirschl Trust

  • Nathaniel B Sawtell

Simons Foundation

  • L F Abbott

Gatsby Charitable Foundation

  • L F Abbott

National Science Foundation (1707398)

  • L F Abbott

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 experiments performed in this study adhere to the American Physiological Society's Guiding Principles in the Care and Use of Animals and were approved by the Columbia University Institutional Animal Care and Use Committee, protocol AAAW4462.

Reviewing Editor

  1. Catherine Emily Carr, University of Maryland, United States

Publication history

  1. Received: November 29, 2018
  2. Accepted: February 21, 2019
  3. Accepted Manuscript published: March 12, 2019 (version 1)
  4. Accepted Manuscript updated: March 14, 2019 (version 2)

Copyright

© 2019, Dempsey 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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