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...

Full description

Bibliographic Details
Main Authors: Charidimos Tzagarakis, Andrew Thompson, Robert D. Rogers, Giuseppe Pellizzer
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-01-01
Series:Frontiers in Integrative Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnint.2019.00001/full
id doaj-cf9fc3672e1a4977bcc700def5b6003f
record_format Article
spelling doaj-cf9fc3672e1a4977bcc700def5b6003f2020-11-25T01:48:38ZengFrontiers Media S.A.Frontiers in Integrative Neuroscience1662-51452019-01-011310.3389/fnint.2019.00001379712The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait ImpulsivityCharidimos Tzagarakis0Charidimos Tzagarakis1Charidimos Tzagarakis2Andrew Thompson3Robert D. Rogers4Robert D. Rogers5Robert D. Rogers6Giuseppe Pellizzer7Giuseppe Pellizzer8Giuseppe Pellizzer9Department of Neuroscience, University of Minnesota, Minneapolis, MN, United StatesBrain Sciences Center, Minneapolis VA Health Care System, Minneapolis, MN, United StatesDepartment of Psychiatry, Warneford Hospital, University of Oxford, Oxford, United KingdomCollege of Biological Sciences, University of Minnesota, Minneapolis, MN, United StatesDepartment of Psychiatry, Warneford Hospital, University of Oxford, Oxford, United KingdomSchool of Psychology, Bangor University, Bangor, United KingdomDepartment of Experimental Psychology, University of Oxford, Oxford, United KingdomDepartment of Neuroscience, University of Minnesota, Minneapolis, MN, United StatesBrain Sciences Center, Minneapolis VA Health Care System, Minneapolis, MN, United StatesDepartment of Neurology, University of Minnesota, Minneapolis, MN, United StatesImpulsivity 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.https://www.frontiersin.org/article/10.3389/fnint.2019.00001/fullimpulsivenessmagnetoencephalographybeta bandmotor cortexmotor planning
collection DOAJ
language English
format Article
sources DOAJ
author Charidimos Tzagarakis
Charidimos Tzagarakis
Charidimos Tzagarakis
Andrew Thompson
Robert D. Rogers
Robert D. Rogers
Robert D. Rogers
Giuseppe Pellizzer
Giuseppe Pellizzer
Giuseppe Pellizzer
spellingShingle Charidimos Tzagarakis
Charidimos Tzagarakis
Charidimos Tzagarakis
Andrew Thompson
Robert D. Rogers
Robert D. Rogers
Robert D. Rogers
Giuseppe Pellizzer
Giuseppe Pellizzer
Giuseppe Pellizzer
The Degree of Modulation of Beta Band Activity During Motor Planning Is Related to Trait Impulsivity
Frontiers in Integrative Neuroscience
impulsiveness
magnetoencephalography
beta band
motor cortex
motor planning
author_facet Charidimos Tzagarakis
Charidimos Tzagarakis
Charidimos Tzagarakis
Andrew Thompson
Robert D. Rogers
Robert D. Rogers
Robert D. Rogers
Giuseppe Pellizzer
Giuseppe Pellizzer
Giuseppe Pellizzer
author_sort Charidimos Tzagarakis
title 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_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_sort degree of modulation of beta band activity during motor planning is related to trait impulsivity
publisher Frontiers Media S.A.
series Frontiers in Integrative Neuroscience
issn 1662-5145
publishDate 2019-01-01
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.
topic impulsiveness
magnetoencephalography
beta band
motor cortex
motor planning
url https://www.frontiersin.org/article/10.3389/fnint.2019.00001/full
work_keys_str_mv AT charidimostzagarakis thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT charidimostzagarakis thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT charidimostzagarakis thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT andrewthompson thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT robertdrogers thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT robertdrogers thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT robertdrogers thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT giuseppepellizzer thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT giuseppepellizzer thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT giuseppepellizzer thedegreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT charidimostzagarakis degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT charidimostzagarakis degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT charidimostzagarakis degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT andrewthompson degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT robertdrogers degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT robertdrogers degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT robertdrogers degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT giuseppepellizzer degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT giuseppepellizzer degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
AT giuseppepellizzer degreeofmodulationofbetabandactivityduringmotorplanningisrelatedtotraitimpulsivity
_version_ 1725011062438232064