Synaptic and intrinsic mechanisms underlying development of cortical direction selectivity

Abstract

Modifications of synaptic inputs and cell-intrinsic properties both contribute to neuronal plasticity and development. To better understand these mechanisms, we undertook an intracellular analysis of the development of direction selectivity in the ferret visual cortex, which occurs rapidly over a few days after eye opening. We found strong evidence of developmental changes in linear spatiotemporal receptive fields of simple cells, implying alterations in circuit inputs. Further, this receptive field plasticity was accompanied by increases in near-spike-threshold excitability and input-output gain that resulted in dramatically increased spiking responses in the experienced state. Increases in subthreshold membrane responses induced by the receptive field plasticity and the increased input-output spiking gain were both necessary to explain the elevated firing rates in experienced ferrets. These results demonstrate that cortical direction selectivity develops through a combination of plasticity in inputs and in cell-intrinsic properties.

Data availability

Data is available at our website at http://data.vhlab.org. Code is available at http://code.vhlab.org (links to GitHub).

Article and author information

Author details

  1. Arani Roy

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jason J Osik

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Benyamin Meschede-Krasa

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Wesley T Alford

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Daniel P Leman

    Department of Biology, Brandeis University, Waltham, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Stephen D Van Hooser

    Department of Biology, Brandeis University, Waltham, United States
    For correspondence
    vanhoosr@brandeis.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1112-5832

Funding

National Eye Institute (EY022122)

  • Arani Roy
  • Jason J Osik
  • Benyamin Meschede-Krasa
  • Wesley T Alford
  • Daniel P Leman
  • Stephen D Van Hooser

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 strict 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 of Brandeis University (19010, 16003, 13011). All procedures were performed under isoflurane anesthesia and every effort was made to minimize suffering.

Copyright

© 2020, Roy 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

  • 1,981
    views
  • 240
    downloads
  • 10
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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)

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

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

  1. Arani Roy
  2. Jason J Osik
  3. Benyamin Meschede-Krasa
  4. Wesley T Alford
  5. Daniel P Leman
  6. Stephen D Van Hooser
(2020)
Synaptic and intrinsic mechanisms underlying development of cortical direction selectivity
eLife 9:e58509.
https://doi.org/10.7554/eLife.58509

Share this article

https://doi.org/10.7554/eLife.58509