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Characterizing neurocognitive impairments in Parkinson’s disease with mobile EEG when walking and stepping over obstacles

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Title: Characterizing neurocognitive impairments in Parkinson’s disease with mobile EEG when walking and stepping over obstacles
Authors: Magda Mustile, Dimitrios Kourtis, Martin G Edwards, Simon Ladouce, Daniele Volpe, Manuela Pilleri, Elisa Pelosin, Gemma Learmonth, David I Donaldson, Magdalena Ietswaart
Contributors: UCL - SSH/IPSY - Psychological Sciences Research Institute, University of St Andrews.School of Psychology and Neuroscience, The Wellcome Trust, SFC Scottish Funding Council, Psychology, Catholic University of Louvain, KU Leuven, Villa Margherita, Fresco Parkinson Center, Ospedale Policlinico San Martino, University of St Andrews, orcid:0000-0002-7903-3184, orcid:0000-0003-2535-6196, orcid:0000-0003-4532-2436, orcid:0000-0002-9880-2241, orcid:0000-0003-4061-4464, orcid:0000-0002-8036-3455, orcid:0000-0003-4576-9393
Source: Brain Commun
Brain Communications, Vol. 5, no.6, p. 2632-1297 (2023)
Publisher Information: Oxford University Press (OUP), 2023.
Publication Year: 2023
Subject Terms: Parkinson's disease, brain oscillations, BETA-BAND OSCILLATIONS, Clinical Neurology, MINI-MENTAL-STATE, gait, MOTOR IMAGERY, ACTIVATION, Cellular and Molecular Neuroscience, obstacle avoidance, SDG 3 - Good Health and Well-being, PEOPLE, Mobile EEG, cognitive control, FRONTAL-MIDLINE THETA, Biological Psychiatry, MCC, Science & Technology, DESYNCHRONIZATION, Neurosciences, 3202 Clinical sciences, DAS, Obstacle avoidance, 16. Peace & justice, 3. Good health, Psychiatry and Mental health, REPETITIVE MOVEMENT, Neurology, GAIT DISORDERS, 5202 Biological psychology, Cognitive control, 3209 Neurosciences, RC0321, Original Article, Neurosciences & Neurology, RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry, Life Sciences & Biomedicine, CORTICAL OSCILLATIONS
Description: The neural correlates that help us understand the challenges that Parkinson’s patients face when negotiating their environment remain under-researched. This deficit in knowledge reflects the methodological constraints of traditional neuroimaging techniques, which include the need to remain still. As a result, much of our understanding of motor disorders is still based on animal models. Daily life challenges such as tripping and falling over obstacles represent one of the main causes of hospitalization for individuals with Parkinson’s disease. Here, we report the neural correlates of naturalistic ambulatory obstacle avoidance in Parkinson’s disease patients using mobile EEG. We examined 14 medicated patients with Parkinson’s disease and 17 neurotypical control participants. Brain activity was recorded while participants walked freely, and while they walked and adjusted their gait to step over expected obstacles (preset adjustment) or unexpected obstacles (online adjustment) displayed on the floor. EEG analysis revealed attenuated cortical activity in Parkinson’s patients compared to neurotypical participants in theta (4–7 Hz) and beta (13–35 Hz) frequency bands. The theta power increase when planning an online adjustment to step over unexpected obstacles was reduced in Parkinson’s patients compared to neurotypical participants, indicating impaired proactive cognitive control of walking that updates the online action plan when unexpected changes occur in the environment. Impaired action planning processes were further evident in Parkinson’s disease patients’ diminished beta power suppression when preparing motor adaptation to step over obstacles, regardless of the expectation manipulation, compared to when walking freely. In addition, deficits in reactive control mechanisms in Parkinson’s disease compared to neurotypical participants were evident from an attenuated beta rebound signal after crossing an obstacle. Reduced modulation in the theta frequency band in the resetting phase across conditions also suggests a deficit in the evaluation of action outcomes in Parkinson’s disease. Taken together, the neural markers of cognitive control of walking observed in Parkinson’s disease reveal a pervasive deficit of motor–cognitive control, involving impairments in the proactive and reactive strategies used to avoid obstacles while walking. As such, this study identified neural markers of the motor deficits in Parkinson’s disease and revealed patients’ difficulties in adapting movements both before and after avoiding obstacles in their path.
Document Type: Article
Other literature type
File Description: application/pdf
Language: English
ISSN: 2632-1297
DOI: 10.1093/braincomms/fcad326
Access URL: https://pubmed.ncbi.nlm.nih.gov/38107501
https://hdl.handle.net/2078.1/288846
https://hdl.handle.net/10023/28888
Rights: CC BY
URL: http://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
Accession Number: edsair.doi.dedup.....dd7ded3ffa090c3e55e256bc3dc96265
Database: OpenAIRE
Description
Abstract:The neural correlates that help us understand the challenges that Parkinson’s patients face when negotiating their environment remain under-researched. This deficit in knowledge reflects the methodological constraints of traditional neuroimaging techniques, which include the need to remain still. As a result, much of our understanding of motor disorders is still based on animal models. Daily life challenges such as tripping and falling over obstacles represent one of the main causes of hospitalization for individuals with Parkinson’s disease. Here, we report the neural correlates of naturalistic ambulatory obstacle avoidance in Parkinson’s disease patients using mobile EEG. We examined 14 medicated patients with Parkinson’s disease and 17 neurotypical control participants. Brain activity was recorded while participants walked freely, and while they walked and adjusted their gait to step over expected obstacles (preset adjustment) or unexpected obstacles (online adjustment) displayed on the floor. EEG analysis revealed attenuated cortical activity in Parkinson’s patients compared to neurotypical participants in theta (4–7 Hz) and beta (13–35 Hz) frequency bands. The theta power increase when planning an online adjustment to step over unexpected obstacles was reduced in Parkinson’s patients compared to neurotypical participants, indicating impaired proactive cognitive control of walking that updates the online action plan when unexpected changes occur in the environment. Impaired action planning processes were further evident in Parkinson’s disease patients’ diminished beta power suppression when preparing motor adaptation to step over obstacles, regardless of the expectation manipulation, compared to when walking freely. In addition, deficits in reactive control mechanisms in Parkinson’s disease compared to neurotypical participants were evident from an attenuated beta rebound signal after crossing an obstacle. Reduced modulation in the theta frequency band in the resetting phase across conditions also suggests a deficit in the evaluation of action outcomes in Parkinson’s disease. Taken together, the neural markers of cognitive control of walking observed in Parkinson’s disease reveal a pervasive deficit of motor–cognitive control, involving impairments in the proactive and reactive strategies used to avoid obstacles while walking. As such, this study identified neural markers of the motor deficits in Parkinson’s disease and revealed patients’ difficulties in adapting movements both before and after avoiding obstacles in their path.
ISSN:26321297
DOI:10.1093/braincomms/fcad326