Laminar microcircuitry of visual cortex producing attention-associated electric fields

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 h...

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Main Authors: Jacob A Westerberg, Michelle S Schall, Alexander Maier, Geoffrey F Woodman, Jeffrey D Schall
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-01-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/72139
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author Jacob A Westerberg
Michelle S Schall
Alexander Maier
Geoffrey F Woodman
Jeffrey D Schall
author_facet Jacob A Westerberg
Michelle S Schall
Alexander Maier
Geoffrey F Woodman
Jeffrey D Schall
author_sort Jacob A Westerberg
collection DOAJ
description 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. Last, 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.
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spelling doaj.art-407d1415f6b845cebe0784d2c3dc6be72022-12-22T04:32:46ZengeLife Sciences Publications LtdeLife2050-084X2022-01-011110.7554/eLife.72139Laminar microcircuitry of visual cortex producing attention-associated electric fieldsJacob A Westerberg0https://orcid.org/0000-0001-5331-8707Michelle S Schall1https://orcid.org/0000-0003-3631-5541Alexander Maier2https://orcid.org/0000-0002-7250-502XGeoffrey F Woodman3https://orcid.org/0000-0003-0946-9297Jeffrey D Schall4https://orcid.org/0000-0002-5248-943XDepartment of Psychology, Center for Integrative and Cognitive Neuroscience, Vanderbilt Vision Research Center, Vanderbilt Brain Institute, Vanderbilt University, Nashville, United StatesDepartment of Psychology, Center for Integrative and Cognitive Neuroscience, Vanderbilt Vision Research Center, Vanderbilt Brain Institute, Vanderbilt University, Nashville, United StatesDepartment of Psychology, Center for Integrative and Cognitive Neuroscience, Vanderbilt Vision Research Center, Vanderbilt Brain Institute, Vanderbilt University, Nashville, United StatesDepartment of Psychology, Center for Integrative and Cognitive Neuroscience, Vanderbilt Vision Research Center, Vanderbilt Brain Institute, Vanderbilt University, Nashville, United StatesCentre for Vision Research, Vision: Science to Applications Program, Departments of Biology and Psychology, York University, Toronto, CanadaCognitive 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. Last, 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.https://elifesciences.org/articles/72139CSDECoGEEGLFPN2pcV4
spellingShingle Jacob A Westerberg
Michelle S Schall
Alexander Maier
Geoffrey F Woodman
Jeffrey D Schall
Laminar microcircuitry of visual cortex producing attention-associated electric fields
eLife
CSD
ECoG
EEG
LFP
N2pc
V4
title Laminar microcircuitry of visual cortex producing attention-associated electric fields
title_full Laminar microcircuitry of visual cortex producing attention-associated electric fields
title_fullStr Laminar microcircuitry of visual cortex producing attention-associated electric fields
title_full_unstemmed Laminar microcircuitry of visual cortex producing attention-associated electric fields
title_short Laminar microcircuitry of visual cortex producing attention-associated electric fields
title_sort laminar microcircuitry of visual cortex producing attention associated electric fields
topic CSD
ECoG
EEG
LFP
N2pc
V4
url https://elifesciences.org/articles/72139
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AT geoffreyfwoodman laminarmicrocircuitryofvisualcortexproducingattentionassociatedelectricfields
AT jeffreydschall laminarmicrocircuitryofvisualcortexproducingattentionassociatedelectricfields