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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Format: | Article |
Language: | English |
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eLife Sciences Publications Ltd
2022-01-01
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Series: | eLife |
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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. |
first_indexed | 2024-04-11T09:01:33Z |
format | Article |
id | doaj.art-407d1415f6b845cebe0784d2c3dc6be7 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-04-11T09:01:33Z |
publishDate | 2022-01-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
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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