Endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobe

Abstract The degree of synchronized fluctuations in neocortical network activity can vary widely during alertness. One influential idea that has emerged over the past few decades is that perceptual decisions are more accurate when the state of population activity is desynchronized. This suggests tha...

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Main Authors: Arun Parajuli, Diego Gutnisky, Nitin Tandon, Valentin Dragoi
Format: Article
Language:English
Published: Nature Portfolio 2023-09-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-41406-3
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author Arun Parajuli
Diego Gutnisky
Nitin Tandon
Valentin Dragoi
author_facet Arun Parajuli
Diego Gutnisky
Nitin Tandon
Valentin Dragoi
author_sort Arun Parajuli
collection DOAJ
description Abstract The degree of synchronized fluctuations in neocortical network activity can vary widely during alertness. One influential idea that has emerged over the past few decades is that perceptual decisions are more accurate when the state of population activity is desynchronized. This suggests that optimal task performance may occur during a particular cortical state – the desynchronized state. Here we show that, contrary to this view, cortical state can both facilitate and suppress perceptual performance in a task-dependent manner. We performed electrical recordings from surface-implanted grid electrodes in the temporal lobe while human subjects completed two perceptual tasks. We found that when local population activity is in a synchronized state, network and perceptual performance are enhanced in a detection task and impaired in a discrimination task, but these modulatory effects are reversed when population activity is desynchronized. These findings indicate that the brain has adapted to take advantage of endogenous fluctuations in the state of neural populations in temporal cortex to selectively enhance different modes of sensory processing during perception in a state-dependent manner.
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spelling doaj.art-1153864dc7aa43bfbf57a5a7452a99452023-11-20T10:07:52ZengNature PortfolioNature Communications2041-17232023-09-0114111110.1038/s41467-023-41406-3Endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobeArun Parajuli0Diego Gutnisky1Nitin Tandon2Valentin Dragoi3Department of Neurobiology and Anatomy, McGovern Medical School, University of Texas at HoustonDepartment of Neurobiology and Anatomy, McGovern Medical School, University of Texas at HoustonVivian L. Smith Department of Neurosurgery, University of Texas Medical SchoolDepartment of Neurobiology and Anatomy, McGovern Medical School, University of Texas at HoustonAbstract The degree of synchronized fluctuations in neocortical network activity can vary widely during alertness. One influential idea that has emerged over the past few decades is that perceptual decisions are more accurate when the state of population activity is desynchronized. This suggests that optimal task performance may occur during a particular cortical state – the desynchronized state. Here we show that, contrary to this view, cortical state can both facilitate and suppress perceptual performance in a task-dependent manner. We performed electrical recordings from surface-implanted grid electrodes in the temporal lobe while human subjects completed two perceptual tasks. We found that when local population activity is in a synchronized state, network and perceptual performance are enhanced in a detection task and impaired in a discrimination task, but these modulatory effects are reversed when population activity is desynchronized. These findings indicate that the brain has adapted to take advantage of endogenous fluctuations in the state of neural populations in temporal cortex to selectively enhance different modes of sensory processing during perception in a state-dependent manner.https://doi.org/10.1038/s41467-023-41406-3
spellingShingle Arun Parajuli
Diego Gutnisky
Nitin Tandon
Valentin Dragoi
Endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobe
Nature Communications
title Endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobe
title_full Endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobe
title_fullStr Endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobe
title_full_unstemmed Endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobe
title_short Endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobe
title_sort endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobe
url https://doi.org/10.1038/s41467-023-41406-3
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AT nitintandon endogenousfluctuationsincorticalstateselectivelyenhancedifferentmodesofsensoryprocessinginhumantemporallobe
AT valentindragoi endogenousfluctuationsincorticalstateselectivelyenhancedifferentmodesofsensoryprocessinginhumantemporallobe