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

Mustile, M., Kourtis, D., Edwards, M. G., Ladouce, S., Volpe, D., Pilleri, M., Pelosin, E., Learmonth, G. , Donaldson, D. I. and Ietswaart, M. (2023) Characterizing neurocognitive impairments in Parkinson’s disease with mobile EEG when walking and stepping over obstacles. Brain Communications, 5(6), fcad326. (doi: 10.1093/braincomms/fcad326) (PMID:38107501) (PMCID:PMC10724048)

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.

• Item Type: Articles
• Additional Information: This work is supported by a scholarship from the University of Stirling and a research grant from SINAPSE (Scottish Imaging Network: A Platform for Scientific excellence). GL is supported by the Wellcome Trust [209209/Z/17/Z].
• Keywords: mobile EEG, Parkinson’s disease, obstacle avoidance, cognitive control.
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Learmonth, Dr Gemma
• Authors: Mustile, M., Kourtis, D., Edwards, M. G., Ladouce, S., Volpe, D., Pilleri, M., Pelosin, E., Learmonth, G., Donaldson, D. I., and Ietswaart, M.
• College/School: College of Medical Veterinary and Life Sciences > School of Psychology & Neuroscience
• Journal Name: Brain Communications
• Publisher: Oxford University Press
• ISSN: 2632-1297
• ISSN (Online): 2632-1297
• Published Online: 28 November 2023
• Copyright Holders: Copyright © 2023 The Author(s)
• First Published: First published in Brain Communications 5(6):fcad326
• Publisher Policy: Reproduced under a Creative Commons license

Project Code	Award No	Project Name	Principal Investigator	Funder's Name	Funder Ref	Lead Dept
300911		Brain Rhythms in Altered Vision after Stroke (BRAVAS)	Gemma Learmonth	Wellcome Trust (WELLCOTR)	209209/Z/17/Z	SPN - Centre for Cognitive Neuroimaging (CCNi)