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The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity

Impulsivity is a prominent personality trait, and a key modulating component of neurologic and psychiatric disorders. How impulsivity is related to the brain mechanisms associated with action planning is poorly understood. Here, we investigated the relation between impulsivity and the modulation of...

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Autores principales: Tzagarakis, Charidimos, Thompson, Andrew, Rogers, Robert D., Pellizzer, Giuseppe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6344424/
https://www.ncbi.nlm.nih.gov/pubmed/30705624
http://dx.doi.org/10.3389/fnint.2019.00001
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author Tzagarakis, Charidimos
Thompson, Andrew
Rogers, Robert D.
Pellizzer, Giuseppe
author_facet Tzagarakis, Charidimos
Thompson, Andrew
Rogers, Robert D.
Pellizzer, Giuseppe
author_sort Tzagarakis, Charidimos
collection PubMed
description Impulsivity is a prominent personality trait, and a key modulating component of neurologic and psychiatric disorders. How impulsivity is related to the brain mechanisms associated with action planning is poorly understood. Here, we investigated the relation between impulsivity and the modulation of beta band oscillatory activity associated with action planning and execution. Given that beta power decreases during action planning and decreases further during action execution, we hypothesized that during planning the level of beta band power of more impulsive individuals would be closer to the level reached during execution than that of less impulsive individuals. This could explain the tendency to “jump the gun” (commission errors) in high impulsivity. To test this hypothesis, we recruited healthy volunteers (50 participants analyzed) and used the Barratt Impulsiveness Scale questionnaire to evaluate their impulsivity as high or low. We then recorded their brain neuromagnetic signals while they performed an instructed-delay task that induced different levels of action planning by varying the number of spatial cues, hence the uncertainty, about the location of the upcoming target. During the early cue period of the task, we found a posterior (source localized in the occipito-parietal areas) and a left fronto-central group of channels (source localized in the left sensorimotor areas) where beta power was modulated by number of cues, whereas during the late cue period only the left fronto-central group was modulated. We found that the decrease of relative beta band power during action planning in the left fronto-central group of channels was more pronounced in the high impulsivity group than in the low impulsivity group. In addition, we found that the beta band-mediated functional connectivity between the posterior and the left fronto-central groups of channels was weaker in the high impulsivity group than in the low impulsivity group during the early cue period. Furthermore, high impulsives made more commission and movement errors in the task than low impulsives. These results reveal neural mechanisms through which impulsivity affects action planning and open the way for further study of the role of beta band activity in impulsivity, especially in the context of disease and therapeutics.
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spelling pubmed-63444242019-01-31 The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity Tzagarakis, Charidimos Thompson, Andrew Rogers, Robert D. Pellizzer, Giuseppe Front Integr Neurosci Neuroscience Impulsivity is a prominent personality trait, and a key modulating component of neurologic and psychiatric disorders. How impulsivity is related to the brain mechanisms associated with action planning is poorly understood. Here, we investigated the relation between impulsivity and the modulation of beta band oscillatory activity associated with action planning and execution. Given that beta power decreases during action planning and decreases further during action execution, we hypothesized that during planning the level of beta band power of more impulsive individuals would be closer to the level reached during execution than that of less impulsive individuals. This could explain the tendency to “jump the gun” (commission errors) in high impulsivity. To test this hypothesis, we recruited healthy volunteers (50 participants analyzed) and used the Barratt Impulsiveness Scale questionnaire to evaluate their impulsivity as high or low. We then recorded their brain neuromagnetic signals while they performed an instructed-delay task that induced different levels of action planning by varying the number of spatial cues, hence the uncertainty, about the location of the upcoming target. During the early cue period of the task, we found a posterior (source localized in the occipito-parietal areas) and a left fronto-central group of channels (source localized in the left sensorimotor areas) where beta power was modulated by number of cues, whereas during the late cue period only the left fronto-central group was modulated. We found that the decrease of relative beta band power during action planning in the left fronto-central group of channels was more pronounced in the high impulsivity group than in the low impulsivity group. In addition, we found that the beta band-mediated functional connectivity between the posterior and the left fronto-central groups of channels was weaker in the high impulsivity group than in the low impulsivity group during the early cue period. Furthermore, high impulsives made more commission and movement errors in the task than low impulsives. These results reveal neural mechanisms through which impulsivity affects action planning and open the way for further study of the role of beta band activity in impulsivity, especially in the context of disease and therapeutics. Frontiers Media S.A. 2019-01-17 /pmc/articles/PMC6344424/ /pubmed/30705624 http://dx.doi.org/10.3389/fnint.2019.00001 Text en Copyright © 2019 Tzagarakis, Thompson, Rogers and Pellizzer. http://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 Neuroscience
Tzagarakis, Charidimos
Thompson, Andrew
Rogers, Robert D.
Pellizzer, Giuseppe
The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity
title The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity
title_full The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity
title_fullStr The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity
title_full_unstemmed The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity
title_short The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity
title_sort degree of modulation of beta band activity during motor planning is related to trait impulsivity
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6344424/
https://www.ncbi.nlm.nih.gov/pubmed/30705624
http://dx.doi.org/10.3389/fnint.2019.00001
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