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.

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.

Metrics

  • 1,277
    views
  • 205
    downloads
  • 15
    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. 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

Share this article

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

Further reading

    1. Neuroscience
    Samyogita Hardikar, Bronte Mckeown ... Jonathan Smallwood
    Research Article

    Complex macro-scale patterns of brain activity that emerge during periods of wakeful rest provide insight into the organisation of neural function, how these differentiate individuals based on their traits, and the neural basis of different types of self-generated thoughts. Although brain activity during wakeful rest is valuable for understanding important features of human cognition, its unconstrained nature makes it difficult to disentangle neural features related to personality traits from those related to the thoughts occurring at rest. Our study builds on recent perspectives from work on ongoing conscious thought that highlight the interactions between three brain networks – ventral and dorsal attention networks, as well as the default mode network. We combined measures of personality with state-of-the-art indices of ongoing thoughts at rest and brain imaging analysis and explored whether this ‘tri-partite’ view can provide a framework within which to understand the contribution of states and traits to observed patterns of neural activity at rest. To capture macro-scale relationships between different brain systems, we calculated cortical gradients to describe brain organisation in a low-dimensional space. Our analysis established that for more introverted individuals, regions of the ventral attention network were functionally more aligned to regions of the somatomotor system and the default mode network. At the same time, a pattern of detailed self-generated thought was associated with a decoupling of regions of dorsal attention from regions in the default mode network. Our study, therefore, establishes that interactions between attention systems and the default mode network are important influences on ongoing thought at rest and highlights the value of integrating contemporary perspectives on conscious experience when understanding patterns of brain activity at rest.

    1. Medicine
    2. Neuroscience
    LeYuan Gu, WeiHui Shao ... HongHai Zhang
    Research Article

    The advent of midazolam holds profound implications for modern clinical practice. The hypnotic and sedative effects of midazolam afford it broad clinical applicability. However, the specific mechanisms underlying the modulation of altered consciousness by midazolam remain elusive. Herein, using pharmacology, optogenetics, chemogenetics, fiber photometry, and gene knockdown, this in vivo research revealed the role of locus coeruleus (LC)-ventrolateral preoptic nucleus noradrenergic neural circuit in regulating midazolam-induced altered consciousness. This effect was mediated by α1 adrenergic receptors. Moreover, gamma-aminobutyric acid receptor type A (GABAA-R) represents a mechanistically crucial binding site in the LC for midazolam. These findings will provide novel insights into the neural circuit mechanisms underlying the recovery of consciousness after midazolam administration and will help guide the timing of clinical dosing and propose effective intervention targets for timely recovery from midazolam-induced loss of consciousness.