Impulsivity in Parkinson’s Disease Is Associated With Alterations in Affective and Sensorimotor Striatal Networks

A subset of patients with Parkinson’s disease (PD) experiences problems with impulse control, characterized by a loss of voluntary control over impulses, drives, or temptations regarding excessive hedonic behavior. The present study aimed to better understand the neural basis of such impulse control...

Full description

Bibliographic Details
Main Authors: Marit F. L. Ruitenberg, Tina Wu, Bruno B. Averbeck, Kelvin L. Chou, Vincent Koppelmans, Rachael D. Seidler
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-04-01
Series:Frontiers in Neurology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fneur.2018.00279/full
_version_ 1818944384902627328
author Marit F. L. Ruitenberg
Tina Wu
Bruno B. Averbeck
Kelvin L. Chou
Vincent Koppelmans
Rachael D. Seidler
Rachael D. Seidler
author_facet Marit F. L. Ruitenberg
Tina Wu
Bruno B. Averbeck
Kelvin L. Chou
Vincent Koppelmans
Rachael D. Seidler
Rachael D. Seidler
author_sort Marit F. L. Ruitenberg
collection DOAJ
description A subset of patients with Parkinson’s disease (PD) experiences problems with impulse control, characterized by a loss of voluntary control over impulses, drives, or temptations regarding excessive hedonic behavior. The present study aimed to better understand the neural basis of such impulse control disorders (ICDs) in PD. We collected resting-state functional connectivity and structural MRI data from 21 PD patients with ICDs and 30 patients without such disorders. To assess impulsivity, all patients completed the Barratt Impulsiveness Scale and performed an information-gathering task. MRI results demonstrated substantial differences in neural characteristics between PD patients with and without ICDs. Results showed that impulsivity was linked to alterations in affective basal ganglia circuitries. Specifically, reduced frontal–striatal connectivity and GPe volume were associated with more impulsivity. We suggest that these changes affect decision making and result in a preference for risky or inappropriate actions. Results further showed that impulsivity was linked to alterations in sensorimotor striatal networks. Enhanced connectivity within this network and larger putamen volume were associated with more impulsivity. We propose that these changes affect sensorimotor processing such that patients have a greater propensity to act. Our findings suggest that the two mechanisms jointly contribute to impulsive behaviors in PD.
first_indexed 2024-12-20T07:42:22Z
format Article
id doaj.art-0437f707b7024d2da676e6fea9597310
institution Directory Open Access Journal
issn 1664-2295
language English
last_indexed 2024-12-20T07:42:22Z
publishDate 2018-04-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neurology
spelling doaj.art-0437f707b7024d2da676e6fea95973102022-12-21T19:48:05ZengFrontiers Media S.A.Frontiers in Neurology1664-22952018-04-01910.3389/fneur.2018.00279354214Impulsivity in Parkinson’s Disease Is Associated With Alterations in Affective and Sensorimotor Striatal NetworksMarit F. L. Ruitenberg0Tina Wu1Bruno B. Averbeck2Kelvin L. Chou3Vincent Koppelmans4Rachael D. Seidler5Rachael D. Seidler6School of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesSchool of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesNational Institute of Mental Health, Bethesda, MD, United StatesDepartment of Neurology, University of Michigan Health System, Ann Arbor, MI, United StatesSchool of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesSchool of Kinesiology, University of Michigan, Ann Arbor, MI, United StatesDepartment of Psychology, University of Michigan, Ann Arbor, MI, United StatesA subset of patients with Parkinson’s disease (PD) experiences problems with impulse control, characterized by a loss of voluntary control over impulses, drives, or temptations regarding excessive hedonic behavior. The present study aimed to better understand the neural basis of such impulse control disorders (ICDs) in PD. We collected resting-state functional connectivity and structural MRI data from 21 PD patients with ICDs and 30 patients without such disorders. To assess impulsivity, all patients completed the Barratt Impulsiveness Scale and performed an information-gathering task. MRI results demonstrated substantial differences in neural characteristics between PD patients with and without ICDs. Results showed that impulsivity was linked to alterations in affective basal ganglia circuitries. Specifically, reduced frontal–striatal connectivity and GPe volume were associated with more impulsivity. We suggest that these changes affect decision making and result in a preference for risky or inappropriate actions. Results further showed that impulsivity was linked to alterations in sensorimotor striatal networks. Enhanced connectivity within this network and larger putamen volume were associated with more impulsivity. We propose that these changes affect sensorimotor processing such that patients have a greater propensity to act. Our findings suggest that the two mechanisms jointly contribute to impulsive behaviors in PD.http://journal.frontiersin.org/article/10.3389/fneur.2018.00279/fullParkinson’s diseaseimpulsivitybasal gangliaaffective striatumsensorimotor striatum
spellingShingle Marit F. L. Ruitenberg
Tina Wu
Bruno B. Averbeck
Kelvin L. Chou
Vincent Koppelmans
Rachael D. Seidler
Rachael D. Seidler
Impulsivity in Parkinson’s Disease Is Associated With Alterations in Affective and Sensorimotor Striatal Networks
Frontiers in Neurology
Parkinson’s disease
impulsivity
basal ganglia
affective striatum
sensorimotor striatum
title Impulsivity in Parkinson’s Disease Is Associated With Alterations in Affective and Sensorimotor Striatal Networks
title_full Impulsivity in Parkinson’s Disease Is Associated With Alterations in Affective and Sensorimotor Striatal Networks
title_fullStr Impulsivity in Parkinson’s Disease Is Associated With Alterations in Affective and Sensorimotor Striatal Networks
title_full_unstemmed Impulsivity in Parkinson’s Disease Is Associated With Alterations in Affective and Sensorimotor Striatal Networks
title_short Impulsivity in Parkinson’s Disease Is Associated With Alterations in Affective and Sensorimotor Striatal Networks
title_sort impulsivity in parkinson s disease is associated with alterations in affective and sensorimotor striatal networks
topic Parkinson’s disease
impulsivity
basal ganglia
affective striatum
sensorimotor striatum
url http://journal.frontiersin.org/article/10.3389/fneur.2018.00279/full
work_keys_str_mv AT maritflruitenberg impulsivityinparkinsonsdiseaseisassociatedwithalterationsinaffectiveandsensorimotorstriatalnetworks
AT tinawu impulsivityinparkinsonsdiseaseisassociatedwithalterationsinaffectiveandsensorimotorstriatalnetworks
AT brunobaverbeck impulsivityinparkinsonsdiseaseisassociatedwithalterationsinaffectiveandsensorimotorstriatalnetworks
AT kelvinlchou impulsivityinparkinsonsdiseaseisassociatedwithalterationsinaffectiveandsensorimotorstriatalnetworks
AT vincentkoppelmans impulsivityinparkinsonsdiseaseisassociatedwithalterationsinaffectiveandsensorimotorstriatalnetworks
AT rachaeldseidler impulsivityinparkinsonsdiseaseisassociatedwithalterationsinaffectiveandsensorimotorstriatalnetworks
AT rachaeldseidler impulsivityinparkinsonsdiseaseisassociatedwithalterationsinaffectiveandsensorimotorstriatalnetworks