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Latent brain state dynamics distinguish behavioral variability, impaired decision-making, and inattention

Children with Attention Deficit Hyperactivity Disorder (ADHD) have prominent deficits in sustained attention that manifest as elevated intra-individual response variability and poor decision-making. Influential neurocognitive models have linked attentional fluctuations to aberrant brain dynamics, bu...

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Autores principales: Cai, Weidong, Warren, Stacie L., Duberg, Katherine, Pennington, Bruce, Hinshaw, Stephen P., Menon, Vinod
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8589642/
https://www.ncbi.nlm.nih.gov/pubmed/33589738
http://dx.doi.org/10.1038/s41380-021-01022-3
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author Cai, Weidong
Warren, Stacie L.
Duberg, Katherine
Pennington, Bruce
Hinshaw, Stephen P.
Menon, Vinod
author_facet Cai, Weidong
Warren, Stacie L.
Duberg, Katherine
Pennington, Bruce
Hinshaw, Stephen P.
Menon, Vinod
author_sort Cai, Weidong
collection PubMed
description Children with Attention Deficit Hyperactivity Disorder (ADHD) have prominent deficits in sustained attention that manifest as elevated intra-individual response variability and poor decision-making. Influential neurocognitive models have linked attentional fluctuations to aberrant brain dynamics, but these models have not been tested with computationally rigorous procedures. Here we use a Research Domain Criteria approach, drift-diffusion modeling of behavior, and a novel Bayesian Switching Dynamic System unsupervised learning algorithm, with ultrafast temporal resolution (490 ms) whole-brain task-fMRI data, to investigate latent brain state dynamics of salience, frontoparietal, and default mode networks and their relation to response variability, latent decision-making processes, and inattention. Our analyses revealed that occurrence of a task-optimal latent brain state predicted decreased intra-individual response variability and increased evidence accumulation related to decision-making. In contrast, occurrence and dwell time of a non-optimal latent brain state predicted inattention symptoms and furthermore, in a categorical analysis, distinguished children with ADHD from controls. Importantly, functional connectivity between salience and frontoparietal networks predicted rate of evidence accumulation to a decision threshold, whereas functional connectivity between salience and default mode networks predicted inattention. Taken together, our computational modeling reveals dissociable latent brain state features underlying response variability, impaired decision-making, and inattentional symptoms common to ADHD. Our findings provide novel insights into the neurobiology of attention deficits in children.
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spelling pubmed-85896422021-11-23 Latent brain state dynamics distinguish behavioral variability, impaired decision-making, and inattention Cai, Weidong Warren, Stacie L. Duberg, Katherine Pennington, Bruce Hinshaw, Stephen P. Menon, Vinod Mol Psychiatry Article Children with Attention Deficit Hyperactivity Disorder (ADHD) have prominent deficits in sustained attention that manifest as elevated intra-individual response variability and poor decision-making. Influential neurocognitive models have linked attentional fluctuations to aberrant brain dynamics, but these models have not been tested with computationally rigorous procedures. Here we use a Research Domain Criteria approach, drift-diffusion modeling of behavior, and a novel Bayesian Switching Dynamic System unsupervised learning algorithm, with ultrafast temporal resolution (490 ms) whole-brain task-fMRI data, to investigate latent brain state dynamics of salience, frontoparietal, and default mode networks and their relation to response variability, latent decision-making processes, and inattention. Our analyses revealed that occurrence of a task-optimal latent brain state predicted decreased intra-individual response variability and increased evidence accumulation related to decision-making. In contrast, occurrence and dwell time of a non-optimal latent brain state predicted inattention symptoms and furthermore, in a categorical analysis, distinguished children with ADHD from controls. Importantly, functional connectivity between salience and frontoparietal networks predicted rate of evidence accumulation to a decision threshold, whereas functional connectivity between salience and default mode networks predicted inattention. Taken together, our computational modeling reveals dissociable latent brain state features underlying response variability, impaired decision-making, and inattentional symptoms common to ADHD. Our findings provide novel insights into the neurobiology of attention deficits in children. Nature Publishing Group UK 2021-02-15 2021 /pmc/articles/PMC8589642/ /pubmed/33589738 http://dx.doi.org/10.1038/s41380-021-01022-3 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Cai, Weidong
Warren, Stacie L.
Duberg, Katherine
Pennington, Bruce
Hinshaw, Stephen P.
Menon, Vinod
Latent brain state dynamics distinguish behavioral variability, impaired decision-making, and inattention
title Latent brain state dynamics distinguish behavioral variability, impaired decision-making, and inattention
title_full Latent brain state dynamics distinguish behavioral variability, impaired decision-making, and inattention
title_fullStr Latent brain state dynamics distinguish behavioral variability, impaired decision-making, and inattention
title_full_unstemmed Latent brain state dynamics distinguish behavioral variability, impaired decision-making, and inattention
title_short Latent brain state dynamics distinguish behavioral variability, impaired decision-making, and inattention
title_sort latent brain state dynamics distinguish behavioral variability, impaired decision-making, and inattention
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8589642/
https://www.ncbi.nlm.nih.gov/pubmed/33589738
http://dx.doi.org/10.1038/s41380-021-01022-3
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