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The Dual-Task Cost Is Due to Neural Interferences Disrupting the Optimal Spatio-Temporal Dynamics of the Competing Tasks

Dual-tasking is extremely prominent nowadays, despite ample evidence that it comes with a performance cost: the Dual-Task (DT) cost. Neuroimaging studies have established that tasks are more likely to interfere if they rely on common brain regions, but the precise neural origin of the DT cost has pr...

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Autores principales: Mac-Auliffe, Diego, Chatard, Benoit, Petton, Mathilde, Croizé, Anne-Claire, Sipp, Florian, Bontemps, Benjamin, Gannerie, Adrien, Bertrand, Olivier, Rheims, Sylvain, Kahane, Philippe, Lachaux, Jean-Philippe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8416616/
https://www.ncbi.nlm.nih.gov/pubmed/34489652
http://dx.doi.org/10.3389/fnbeh.2021.640178
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author Mac-Auliffe, Diego
Chatard, Benoit
Petton, Mathilde
Croizé, Anne-Claire
Sipp, Florian
Bontemps, Benjamin
Gannerie, Adrien
Bertrand, Olivier
Rheims, Sylvain
Kahane, Philippe
Lachaux, Jean-Philippe
author_facet Mac-Auliffe, Diego
Chatard, Benoit
Petton, Mathilde
Croizé, Anne-Claire
Sipp, Florian
Bontemps, Benjamin
Gannerie, Adrien
Bertrand, Olivier
Rheims, Sylvain
Kahane, Philippe
Lachaux, Jean-Philippe
author_sort Mac-Auliffe, Diego
collection PubMed
description Dual-tasking is extremely prominent nowadays, despite ample evidence that it comes with a performance cost: the Dual-Task (DT) cost. Neuroimaging studies have established that tasks are more likely to interfere if they rely on common brain regions, but the precise neural origin of the DT cost has proven elusive so far, mostly because fMRI does not record neural activity directly and cannot reveal the key effect of timing, and how the spatio-temporal neural dynamics of the tasks coincide. Recently, DT electrophysiological studies in monkeys have recorded neural populations shared by the two tasks with millisecond precision to provide a much finer understanding of the origin of the DT cost. We used a similar approach in humans, with intracranial EEG, to assess the neural origin of the DT cost in a particularly challenging naturalistic paradigm which required accurate motor responses to frequent visual stimuli (task T1) and the retrieval of information from long-term memory (task T2), as when answering passengers’ questions while driving. We found that T2 elicited neuroelectric interferences in the gamma-band (>40 Hz), in key regions of the T1 network including the Multiple Demand Network. They reproduced the effect of disruptive electrocortical stimulations to create a situation of dynamical incompatibility, which might explain the DT cost. Yet, participants were able to flexibly adapt their strategy to minimize interference, and most surprisingly, reduce the reliance of T1 on key regions of the executive control network-the anterior insula and the dorsal anterior cingulate cortex-with no performance decrement.
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spelling pubmed-84166162021-09-05 The Dual-Task Cost Is Due to Neural Interferences Disrupting the Optimal Spatio-Temporal Dynamics of the Competing Tasks Mac-Auliffe, Diego Chatard, Benoit Petton, Mathilde Croizé, Anne-Claire Sipp, Florian Bontemps, Benjamin Gannerie, Adrien Bertrand, Olivier Rheims, Sylvain Kahane, Philippe Lachaux, Jean-Philippe Front Behav Neurosci Behavioral Neuroscience Dual-tasking is extremely prominent nowadays, despite ample evidence that it comes with a performance cost: the Dual-Task (DT) cost. Neuroimaging studies have established that tasks are more likely to interfere if they rely on common brain regions, but the precise neural origin of the DT cost has proven elusive so far, mostly because fMRI does not record neural activity directly and cannot reveal the key effect of timing, and how the spatio-temporal neural dynamics of the tasks coincide. Recently, DT electrophysiological studies in monkeys have recorded neural populations shared by the two tasks with millisecond precision to provide a much finer understanding of the origin of the DT cost. We used a similar approach in humans, with intracranial EEG, to assess the neural origin of the DT cost in a particularly challenging naturalistic paradigm which required accurate motor responses to frequent visual stimuli (task T1) and the retrieval of information from long-term memory (task T2), as when answering passengers’ questions while driving. We found that T2 elicited neuroelectric interferences in the gamma-band (>40 Hz), in key regions of the T1 network including the Multiple Demand Network. They reproduced the effect of disruptive electrocortical stimulations to create a situation of dynamical incompatibility, which might explain the DT cost. Yet, participants were able to flexibly adapt their strategy to minimize interference, and most surprisingly, reduce the reliance of T1 on key regions of the executive control network-the anterior insula and the dorsal anterior cingulate cortex-with no performance decrement. Frontiers Media S.A. 2021-08-19 /pmc/articles/PMC8416616/ /pubmed/34489652 http://dx.doi.org/10.3389/fnbeh.2021.640178 Text en Copyright © 2021 Mac-Auliffe, Chatard, Petton, Croizé, Sipp, Bontemps, Gannerie, Bertrand, Rheims, Kahane and Lachaux. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Behavioral Neuroscience
Mac-Auliffe, Diego
Chatard, Benoit
Petton, Mathilde
Croizé, Anne-Claire
Sipp, Florian
Bontemps, Benjamin
Gannerie, Adrien
Bertrand, Olivier
Rheims, Sylvain
Kahane, Philippe
Lachaux, Jean-Philippe
The Dual-Task Cost Is Due to Neural Interferences Disrupting the Optimal Spatio-Temporal Dynamics of the Competing Tasks
title The Dual-Task Cost Is Due to Neural Interferences Disrupting the Optimal Spatio-Temporal Dynamics of the Competing Tasks
title_full The Dual-Task Cost Is Due to Neural Interferences Disrupting the Optimal Spatio-Temporal Dynamics of the Competing Tasks
title_fullStr The Dual-Task Cost Is Due to Neural Interferences Disrupting the Optimal Spatio-Temporal Dynamics of the Competing Tasks
title_full_unstemmed The Dual-Task Cost Is Due to Neural Interferences Disrupting the Optimal Spatio-Temporal Dynamics of the Competing Tasks
title_short The Dual-Task Cost Is Due to Neural Interferences Disrupting the Optimal Spatio-Temporal Dynamics of the Competing Tasks
title_sort dual-task cost is due to neural interferences disrupting the optimal spatio-temporal dynamics of the competing tasks
topic Behavioral Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8416616/
https://www.ncbi.nlm.nih.gov/pubmed/34489652
http://dx.doi.org/10.3389/fnbeh.2021.640178
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