Subthalamic deep brain stimulation identifies frontal networks supporting initiation, inhibition and strategy use in Parkinson's disease
Initiation and inhibition are executive functions whose disruption in Parkinson's disease impacts substantially on everyday activities. Management of Parkinson's disease with subthalamic deep brain stimulation (DBS) modifies initiation and inhibition, with prior work suggesting that these...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2020-12-01
|
Series: | NeuroImage |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811920308387 |
id |
doaj-232af5270bfc431b89d391f64107044f |
---|---|
record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Philip E. Mosley Katherine Robinson Terry Coyne Peter Silburn Megan S. Barker Michael Breakspear Gail A. Robinson Alistair Perry |
spellingShingle |
Philip E. Mosley Katherine Robinson Terry Coyne Peter Silburn Megan S. Barker Michael Breakspear Gail A. Robinson Alistair Perry Subthalamic deep brain stimulation identifies frontal networks supporting initiation, inhibition and strategy use in Parkinson's disease NeuroImage Deep brain stimulation subthalamic nucleus impulsivity inhibition Parkinson's disease executive functioning |
author_facet |
Philip E. Mosley Katherine Robinson Terry Coyne Peter Silburn Megan S. Barker Michael Breakspear Gail A. Robinson Alistair Perry |
author_sort |
Philip E. Mosley |
title |
Subthalamic deep brain stimulation identifies frontal networks supporting initiation, inhibition and strategy use in Parkinson's disease |
title_short |
Subthalamic deep brain stimulation identifies frontal networks supporting initiation, inhibition and strategy use in Parkinson's disease |
title_full |
Subthalamic deep brain stimulation identifies frontal networks supporting initiation, inhibition and strategy use in Parkinson's disease |
title_fullStr |
Subthalamic deep brain stimulation identifies frontal networks supporting initiation, inhibition and strategy use in Parkinson's disease |
title_full_unstemmed |
Subthalamic deep brain stimulation identifies frontal networks supporting initiation, inhibition and strategy use in Parkinson's disease |
title_sort |
subthalamic deep brain stimulation identifies frontal networks supporting initiation, inhibition and strategy use in parkinson's disease |
publisher |
Elsevier |
series |
NeuroImage |
issn |
1095-9572 |
publishDate |
2020-12-01 |
description |
Initiation and inhibition are executive functions whose disruption in Parkinson's disease impacts substantially on everyday activities. Management of Parkinson's disease with subthalamic deep brain stimulation (DBS) modifies initiation and inhibition, with prior work suggesting that these effects may be mediated via the connectivity of the subthalamic nucleus (STN) with the frontal cortex. Here, we employed high-resolution structural neuroimaging to investigate the variability in initiation, inhibition and strategy use in a cohort of twenty-five (ten females, mean age 62.5, mean Hoehn and Yahr stage 2.5) participants undertaking subthalamic DBS for Parkinson's disease. Neuropsychological assessment of initiation and inhibition was performed preoperatively and at six months postoperatively. We first reconstructed the preoperative connectivity of the STN with a frontal network of anterior and superior medial cortical regions. We then modelled the postoperative site of subthalamic stimulation and reconstructed the connectivity of the stimulation field within this same network. We found that, at both pre- and postoperative intervals, inter-individual variability in inhibition and initiation were strongly associated with structural network connectivity. Measures of subcortical atrophy and local stimulation effects did not play a significant role. Preoperatively, we replicated prior work, including a role for the right inferior frontal gyrus in inhibition and strategy use, as well as the left inferior frontal gyrus in tasks requiring selection under conditions of maintained inhibition. Postoperatively, greater connectivity of the stimulation field with right anterior cortical regions was associated with greater rule violations and suppression errors, supporting prior work implicating right-hemispheric STN stimulation in disinhibition. Our findings suggest that, in Parkinson's disease, connectivity of the frontal cortex with the STN is an important mediator of individual variability in initiation and inhibition,. Personalised information on brain network architecture could guide individualised brain circuit manipulation to minimise neuropsychological disruption after STN-DBS. |
topic |
Deep brain stimulation subthalamic nucleus impulsivity inhibition Parkinson's disease executive functioning |
url |
http://www.sciencedirect.com/science/article/pii/S1053811920308387 |
work_keys_str_mv |
AT philipemosley subthalamicdeepbrainstimulationidentifiesfrontalnetworkssupportinginitiationinhibitionandstrategyuseinparkinsonsdisease AT katherinerobinson subthalamicdeepbrainstimulationidentifiesfrontalnetworkssupportinginitiationinhibitionandstrategyuseinparkinsonsdisease AT terrycoyne subthalamicdeepbrainstimulationidentifiesfrontalnetworkssupportinginitiationinhibitionandstrategyuseinparkinsonsdisease AT petersilburn subthalamicdeepbrainstimulationidentifiesfrontalnetworkssupportinginitiationinhibitionandstrategyuseinparkinsonsdisease AT megansbarker subthalamicdeepbrainstimulationidentifiesfrontalnetworkssupportinginitiationinhibitionandstrategyuseinparkinsonsdisease AT michaelbreakspear subthalamicdeepbrainstimulationidentifiesfrontalnetworkssupportinginitiationinhibitionandstrategyuseinparkinsonsdisease AT gailarobinson subthalamicdeepbrainstimulationidentifiesfrontalnetworkssupportinginitiationinhibitionandstrategyuseinparkinsonsdisease AT alistairperry subthalamicdeepbrainstimulationidentifiesfrontalnetworkssupportinginitiationinhibitionandstrategyuseinparkinsonsdisease |
_version_ |
1724451462051790848 |
spelling |
doaj-232af5270bfc431b89d391f64107044f2020-11-25T04:00:18ZengElsevierNeuroImage1095-95722020-12-01223117352Subthalamic deep brain stimulation identifies frontal networks supporting initiation, inhibition and strategy use in Parkinson's diseasePhilip E. Mosley0Katherine Robinson1Terry Coyne2Peter Silburn3Megan S. Barker4Michael Breakspear5Gail A. Robinson6Alistair Perry7Systems Neuroscience Group, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia; Neurosciences Queensland, St Andrew's War Memorial Hospital, Level 1, St Andrew's Place, 33 North Street, Spring Hill, Queensland 4000, Australia; Queensland Brain Institute, University of Queensland, St Lucia, Queensland, Australia; Faculty of Medicine, University of Queensland, Herston, Queensland, Australia; Corresponding author at: Neurosciences Queensland, St Andrew's War Memorial Hospital, Level 1, St Andrew's Place, 33 North Street, Spring Hill, Queensland 4000, Australia.Systems Neuroscience Group, QIMR Berghofer Medical Research Institute, Herston, Queensland, AustraliaQueensland Brain Institute, University of Queensland, St Lucia, Queensland, Australia; Brizbrain and Spine, the Wesley Hospital, Auchenflower, Queensland, AustraliaNeurosciences Queensland, St Andrew's War Memorial Hospital, Level 1, St Andrew's Place, 33 North Street, Spring Hill, Queensland 4000, Australia; Queensland Brain Institute, University of Queensland, St Lucia, Queensland, AustraliaSchool of Psychology, University of Queensland, St Lucia, Queensland, Australia; Taub Institute for Research on Alzheimer's Disease and the Aging Brain, Columbia University Medical Centre, New York, USASystems Neuroscience Group, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia; Brain and Mind Priority Research Centre, Hunter Medical Research Institute, University of Newcastle, NSW, AustraliaQueensland Brain Institute, University of Queensland, St Lucia, Queensland, Australia; School of Psychology, University of Queensland, St Lucia, Queensland, AustraliaSystems Neuroscience Group, QIMR Berghofer Medical Research Institute, Herston, Queensland, Australia; Max Planck UCL Centre for Computational Psychiatry and Ageing Research, Berlin, Germany; Centre for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, GermanyInitiation and inhibition are executive functions whose disruption in Parkinson's disease impacts substantially on everyday activities. Management of Parkinson's disease with subthalamic deep brain stimulation (DBS) modifies initiation and inhibition, with prior work suggesting that these effects may be mediated via the connectivity of the subthalamic nucleus (STN) with the frontal cortex. Here, we employed high-resolution structural neuroimaging to investigate the variability in initiation, inhibition and strategy use in a cohort of twenty-five (ten females, mean age 62.5, mean Hoehn and Yahr stage 2.5) participants undertaking subthalamic DBS for Parkinson's disease. Neuropsychological assessment of initiation and inhibition was performed preoperatively and at six months postoperatively. We first reconstructed the preoperative connectivity of the STN with a frontal network of anterior and superior medial cortical regions. We then modelled the postoperative site of subthalamic stimulation and reconstructed the connectivity of the stimulation field within this same network. We found that, at both pre- and postoperative intervals, inter-individual variability in inhibition and initiation were strongly associated with structural network connectivity. Measures of subcortical atrophy and local stimulation effects did not play a significant role. Preoperatively, we replicated prior work, including a role for the right inferior frontal gyrus in inhibition and strategy use, as well as the left inferior frontal gyrus in tasks requiring selection under conditions of maintained inhibition. Postoperatively, greater connectivity of the stimulation field with right anterior cortical regions was associated with greater rule violations and suppression errors, supporting prior work implicating right-hemispheric STN stimulation in disinhibition. Our findings suggest that, in Parkinson's disease, connectivity of the frontal cortex with the STN is an important mediator of individual variability in initiation and inhibition,. Personalised information on brain network architecture could guide individualised brain circuit manipulation to minimise neuropsychological disruption after STN-DBS.http://www.sciencedirect.com/science/article/pii/S1053811920308387Deep brain stimulationsubthalamic nucleusimpulsivityinhibitionParkinson's diseaseexecutive functioning |