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Conflict Detection in a Sequential Decision Task Is Associated with Increased Cortico-Subthalamic Coherence and Prolonged Subthalamic Oscillatory Response in the β Band

Making accurate decisions often involves the integration of current and past evidence. Here, we examine the neural correlates of conflict and evidence integration during sequential decision-making. Female and male human patients implanted with deep-brain stimulation (DBS) electrodes and age-matched...

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Autores principales: Patai, E. Zita, Foltynie, Thomas, Limousin, Patricia, Akram, Harith, Zrinzo, Ludvic, Bogacz, Rafal, Litvak, Vladimir
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9186803/
https://www.ncbi.nlm.nih.gov/pubmed/35501153
http://dx.doi.org/10.1523/JNEUROSCI.0572-21.2022
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author Patai, E. Zita
Foltynie, Thomas
Limousin, Patricia
Akram, Harith
Zrinzo, Ludvic
Bogacz, Rafal
Litvak, Vladimir
author_facet Patai, E. Zita
Foltynie, Thomas
Limousin, Patricia
Akram, Harith
Zrinzo, Ludvic
Bogacz, Rafal
Litvak, Vladimir
author_sort Patai, E. Zita
collection PubMed
description Making accurate decisions often involves the integration of current and past evidence. Here, we examine the neural correlates of conflict and evidence integration during sequential decision-making. Female and male human patients implanted with deep-brain stimulation (DBS) electrodes and age-matched and gender-matched healthy controls performed an expanded judgment task, in which they were free to choose how many cues to sample. Behaviorally, we found that while patients sampled numerically more cues, they were less able to integrate evidence and showed suboptimal performance. Using recordings of magnetoencephalography (MEG) and local field potentials (LFPs; in patients) in the subthalamic nucleus (STN), we found that β oscillations signaled conflict between cues within a sequence. Following cues that differed from previous cues, β power in the STN and cortex first decreased and then increased. Importantly, the conflict signal in the STN outlasted the cortical one, carrying over to the next cue in the sequence. Furthermore, after a conflict, there was an increase in coherence between the dorsal premotor cortex and STN in the β band. These results extend our understanding of cortico-subcortical dynamics of conflict processing, and do so in a context where evidence must be accumulated in discrete steps, much like in real life. Thus, the present work leads to a more nuanced picture of conflict monitoring systems in the brain and potential changes because of disease. SIGNIFICANCE STATEMENT Decision-making often involves the integration of multiple pieces of information over time to make accurate predictions. We simultaneously recorded whole-head magnetoencephalography (MEG) and local field potentials (LFPs) from the human subthalamic nucleus (STN) in a novel task which required integrating sequentially presented pieces of evidence. Our key finding is prolonged β oscillations in the STN, with a concurrent increase in communication with frontal cortex, when presented with conflicting information. These neural effects reflect the behavioral profile of reduced tendency to respond after conflict, as well as relate to suboptimal cue integration in patients, which may be directly linked to clinically reported side-effects of deep-brain stimulation (DBS) such as impaired decision-making and impulsivity.
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spelling pubmed-91868032022-06-13 Conflict Detection in a Sequential Decision Task Is Associated with Increased Cortico-Subthalamic Coherence and Prolonged Subthalamic Oscillatory Response in the β Band Patai, E. Zita Foltynie, Thomas Limousin, Patricia Akram, Harith Zrinzo, Ludvic Bogacz, Rafal Litvak, Vladimir J Neurosci Research Articles Making accurate decisions often involves the integration of current and past evidence. Here, we examine the neural correlates of conflict and evidence integration during sequential decision-making. Female and male human patients implanted with deep-brain stimulation (DBS) electrodes and age-matched and gender-matched healthy controls performed an expanded judgment task, in which they were free to choose how many cues to sample. Behaviorally, we found that while patients sampled numerically more cues, they were less able to integrate evidence and showed suboptimal performance. Using recordings of magnetoencephalography (MEG) and local field potentials (LFPs; in patients) in the subthalamic nucleus (STN), we found that β oscillations signaled conflict between cues within a sequence. Following cues that differed from previous cues, β power in the STN and cortex first decreased and then increased. Importantly, the conflict signal in the STN outlasted the cortical one, carrying over to the next cue in the sequence. Furthermore, after a conflict, there was an increase in coherence between the dorsal premotor cortex and STN in the β band. These results extend our understanding of cortico-subcortical dynamics of conflict processing, and do so in a context where evidence must be accumulated in discrete steps, much like in real life. Thus, the present work leads to a more nuanced picture of conflict monitoring systems in the brain and potential changes because of disease. SIGNIFICANCE STATEMENT Decision-making often involves the integration of multiple pieces of information over time to make accurate predictions. We simultaneously recorded whole-head magnetoencephalography (MEG) and local field potentials (LFPs) from the human subthalamic nucleus (STN) in a novel task which required integrating sequentially presented pieces of evidence. Our key finding is prolonged β oscillations in the STN, with a concurrent increase in communication with frontal cortex, when presented with conflicting information. These neural effects reflect the behavioral profile of reduced tendency to respond after conflict, as well as relate to suboptimal cue integration in patients, which may be directly linked to clinically reported side-effects of deep-brain stimulation (DBS) such as impaired decision-making and impulsivity. Society for Neuroscience 2022-06-08 /pmc/articles/PMC9186803/ /pubmed/35501153 http://dx.doi.org/10.1523/JNEUROSCI.0572-21.2022 Text en Copyright © 2022 Patai et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Articles
Patai, E. Zita
Foltynie, Thomas
Limousin, Patricia
Akram, Harith
Zrinzo, Ludvic
Bogacz, Rafal
Litvak, Vladimir
Conflict Detection in a Sequential Decision Task Is Associated with Increased Cortico-Subthalamic Coherence and Prolonged Subthalamic Oscillatory Response in the β Band
title Conflict Detection in a Sequential Decision Task Is Associated with Increased Cortico-Subthalamic Coherence and Prolonged Subthalamic Oscillatory Response in the β Band
title_full Conflict Detection in a Sequential Decision Task Is Associated with Increased Cortico-Subthalamic Coherence and Prolonged Subthalamic Oscillatory Response in the β Band
title_fullStr Conflict Detection in a Sequential Decision Task Is Associated with Increased Cortico-Subthalamic Coherence and Prolonged Subthalamic Oscillatory Response in the β Band
title_full_unstemmed Conflict Detection in a Sequential Decision Task Is Associated with Increased Cortico-Subthalamic Coherence and Prolonged Subthalamic Oscillatory Response in the β Band
title_short Conflict Detection in a Sequential Decision Task Is Associated with Increased Cortico-Subthalamic Coherence and Prolonged Subthalamic Oscillatory Response in the β Band
title_sort conflict detection in a sequential decision task is associated with increased cortico-subthalamic coherence and prolonged subthalamic oscillatory response in the β band
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9186803/
https://www.ncbi.nlm.nih.gov/pubmed/35501153
http://dx.doi.org/10.1523/JNEUROSCI.0572-21.2022
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