Laminar microcircuitry of visual cortex producing attention-associated electric fields

  1. Jacob A Westerberg  Is a corresponding author
  2. Michelle S Schall
  3. Alexander Maier
  4. Geoffrey F Woodman
  5. Jeffrey D Schall
  1. Vanderbilt University, United States
  2. York University, Canada

Abstract

Cognitive operations are widely studied by measuring electric fields through EEG and ECoG. However, despite their widespread use, the neural circuitry giving rise to these signals remains unknown because the functional architecture of cortical columns producing attention-associated electric fields has not been explored. Here we detail the laminar cortical circuitry underlying an attention-associated electric field measured over posterior regions of the brain in humans and monkeys. First, we identified visual cortical area V4 as one plausible contributor to this attention-associated electric field through inverse modeling of cranial EEG in macaque monkeys performing a visual attention task. Next, we performed laminar neurophysiological recordings on the prelunate gyrus and identified the electric-field-producing dipoles as synaptic activity in distinct cortical layers of area V4. Specifically, activation in the extragranular layers of cortex resulted in the generation of the attention-associated dipole. Feature selectivity of a given cortical column determined the overall contribution to this electric field. Columns selective for the attended feature contributed more to the electric field than columns selective for a different feature. Lastly, the laminar profile of synaptic activity generated by V4 was sufficient to produce an attention-associated signal measurable outside of the column. These findings suggest that the top-down recipient cortical layers produce an attention-associated electric field that can be measured extracortically with the relative contribution of each column depending upon the underlying functional architecture.

Data availability

Data supporting the findings documented in this study are freely available online through Dryad at https://doi.org/10.5061/dryad.djh9w0w15.

The following data sets were generated

Article and author information

Author details

  1. Jacob A Westerberg

    Department of Psychology, Vanderbilt University, Nashville, United States
    For correspondence
    jacob.a.westerberg@vanderbilt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5331-8707
  2. Michelle S Schall

    Department of Psychology, Vanderbilt University, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexander Maier

    Department of Psychology, Vanderbilt University, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7250-502X
  4. Geoffrey F Woodman

    Department of Psychology, Vanderbilt University, Nashville, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jeffrey D Schall

    Department of Biology, York University, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Eye Institute (F31EY031293)

  • Jacob A Westerberg

National Eye Institute (P30EY008126)

  • Alexander Maier
  • Geoffrey F Woodman
  • Jeffrey D Schall

National Eye Institute (R01EY019882)

  • Geoffrey F Woodman
  • Jeffrey D Schall

National Eye Institute (R01EY008890)

  • Jeffrey D Schall

National Eye Institute (R01EY027402)

  • Alexander Maier

Office of the Director (S10OD021771)

  • Alexander Maier
  • Geoffrey F Woodman
  • Jeffrey D Schall

National Eye Institute (T32EY007135)

  • Jacob A Westerberg

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

Ethics

Animal experimentation: Procedures were in accordance with National Institutes of Health Guidelines, Association for Assessment and Accreditation of Laboratory Animal Care Guide for the Care and Use of Laboratory Animals, and approved by the Vanderbilt Institutional Animal Care and Use Committee (Protocol M1700067) following United States Department of Agriculture and Public Health Services policies.

Reviewing Editor

  1. Supratim Ray, Indian Institute of Science, India

Version history

  1. Received: July 13, 2021
  2. Preprint posted: September 11, 2021 (view preprint)
  3. Accepted: January 25, 2022
  4. Accepted Manuscript published: January 28, 2022 (version 1)
  5. Version of Record published: February 15, 2022 (version 2)

Copyright

© 2022, Westerberg 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. Jacob A Westerberg
  2. Michelle S Schall
  3. Alexander Maier
  4. Geoffrey F Woodman
  5. Jeffrey D Schall
(2022)
Laminar microcircuitry of visual cortex producing attention-associated electric fields
eLife 11:e72139.
https://doi.org/10.7554/eLife.72139

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https://doi.org/10.7554/eLife.72139

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