Subthalamic and nigral neurons are differentially modulated during parkinsonian gait
The parkinsonian gait disorder and freezing of gait are therapeutically demanding symptoms with considerable impact on quality of life. The aim of this study was to assess the role of subthalamic and nigral neurons in the parkinsonian gait control using intraoperative microelectrode recordings of ba...
Հիմնական հեղինակներ: | , , , , , , , , , , , , , |
---|---|
Ձևաչափ: | Journal article |
Լեզու: | English |
Հրապարակվել է: |
Oxford University Press
2023
|
_version_ | 1826311523790749696 |
---|---|
author | Gulberti, A Wagner, JR Horn, MA Reuss, JH Heise, M Koeppen, JA Pinnschmidt, HO Westphal, M Engel, AK Gerloff, C Sharott, A Hamel, W Moll, CKE Pötter-Nerger, M |
author_facet | Gulberti, A Wagner, JR Horn, MA Reuss, JH Heise, M Koeppen, JA Pinnschmidt, HO Westphal, M Engel, AK Gerloff, C Sharott, A Hamel, W Moll, CKE Pötter-Nerger, M |
author_sort | Gulberti, A |
collection | OXFORD |
description | The parkinsonian gait disorder and freezing of gait are therapeutically demanding symptoms with considerable impact on quality of life. The aim of this study was to assess the role of subthalamic and nigral neurons in the parkinsonian gait control using intraoperative microelectrode recordings of basal ganglia neurons during a supine stepping task. Twelve male patients (56 ± 7 years) suffering from moderate idiopathic Parkinson's disease (disease duration 10 ± 3 years, Hoehn and Yahr stage 2), undergoing awake neurosurgery for deep brain stimulation, participated in the study. After 10 s resting, stepping at self-paced speed for 35 s was followed by short intervals of stepping in response to random 'start' and 'stop' cues. Single- and multi-unit activity was analysed offline in relation to different aspects of the stepping task (attentional 'start' and 'stop' cues, heel strikes, stepping irregularities) in terms of firing frequency, firing pattern and oscillatory activity. Subthalamic nucleus and substantia nigra neurons responded to different aspects of the stepping task. Of the subthalamic nucleus neurons, 24% exhibited movement-related activity modulation as an increase of the firing rate, suggesting a predominant role of the subthalamic nucleus in motor aspects of the task, while 8% of subthalamic nucleus neurons showed a modulation in response to the attentional cues. In contrast, responsive substantia nigra neurons showed activity changes exclusively associated with attentional aspects of the stepping task (15%). The firing pattern of subthalamic nucleus neurons revealed gait-related firing regularization and a drop of beta oscillations during the stepping performance. During freezing episodes instead, there was a rise of beta oscillatory activity. This study shows for the first time specific, task-related subthalamic nucleus and substantia nigra single-unit activity changes during gait-like movements in humans with differential roles in motor and attentional control of gait. The emergence of perturbed firing patterns in the subthalamic nucleus indicates a disrupted information transfer within the gait network, resulting in freezing of gait. |
first_indexed | 2024-03-07T08:11:07Z |
format | Journal article |
id | oxford-uuid:6dd884fe-82ab-4ac8-a9de-c983d216ecec |
institution | University of Oxford |
language | English |
last_indexed | 2024-03-07T08:11:07Z |
publishDate | 2023 |
publisher | Oxford University Press |
record_format | dspace |
spelling | oxford-uuid:6dd884fe-82ab-4ac8-a9de-c983d216ecec2023-11-28T12:22:24ZSubthalamic and nigral neurons are differentially modulated during parkinsonian gaitJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:6dd884fe-82ab-4ac8-a9de-c983d216ececEnglishSymplectic ElementsOxford University Press2023Gulberti, AWagner, JRHorn, MAReuss, JHHeise, MKoeppen, JAPinnschmidt, HOWestphal, MEngel, AKGerloff, CSharott, AHamel, WMoll, CKEPötter-Nerger, MThe parkinsonian gait disorder and freezing of gait are therapeutically demanding symptoms with considerable impact on quality of life. The aim of this study was to assess the role of subthalamic and nigral neurons in the parkinsonian gait control using intraoperative microelectrode recordings of basal ganglia neurons during a supine stepping task. Twelve male patients (56 ± 7 years) suffering from moderate idiopathic Parkinson's disease (disease duration 10 ± 3 years, Hoehn and Yahr stage 2), undergoing awake neurosurgery for deep brain stimulation, participated in the study. After 10 s resting, stepping at self-paced speed for 35 s was followed by short intervals of stepping in response to random 'start' and 'stop' cues. Single- and multi-unit activity was analysed offline in relation to different aspects of the stepping task (attentional 'start' and 'stop' cues, heel strikes, stepping irregularities) in terms of firing frequency, firing pattern and oscillatory activity. Subthalamic nucleus and substantia nigra neurons responded to different aspects of the stepping task. Of the subthalamic nucleus neurons, 24% exhibited movement-related activity modulation as an increase of the firing rate, suggesting a predominant role of the subthalamic nucleus in motor aspects of the task, while 8% of subthalamic nucleus neurons showed a modulation in response to the attentional cues. In contrast, responsive substantia nigra neurons showed activity changes exclusively associated with attentional aspects of the stepping task (15%). The firing pattern of subthalamic nucleus neurons revealed gait-related firing regularization and a drop of beta oscillations during the stepping performance. During freezing episodes instead, there was a rise of beta oscillatory activity. This study shows for the first time specific, task-related subthalamic nucleus and substantia nigra single-unit activity changes during gait-like movements in humans with differential roles in motor and attentional control of gait. The emergence of perturbed firing patterns in the subthalamic nucleus indicates a disrupted information transfer within the gait network, resulting in freezing of gait. |
spellingShingle | Gulberti, A Wagner, JR Horn, MA Reuss, JH Heise, M Koeppen, JA Pinnschmidt, HO Westphal, M Engel, AK Gerloff, C Sharott, A Hamel, W Moll, CKE Pötter-Nerger, M Subthalamic and nigral neurons are differentially modulated during parkinsonian gait |
title | Subthalamic and nigral neurons are differentially modulated during parkinsonian gait |
title_full | Subthalamic and nigral neurons are differentially modulated during parkinsonian gait |
title_fullStr | Subthalamic and nigral neurons are differentially modulated during parkinsonian gait |
title_full_unstemmed | Subthalamic and nigral neurons are differentially modulated during parkinsonian gait |
title_short | Subthalamic and nigral neurons are differentially modulated during parkinsonian gait |
title_sort | subthalamic and nigral neurons are differentially modulated during parkinsonian gait |
work_keys_str_mv | AT gulbertia subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT wagnerjr subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT hornma subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT reussjh subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT heisem subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT koeppenja subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT pinnschmidtho subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT westphalm subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT engelak subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT gerloffc subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT sharotta subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT hamelw subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT mollcke subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait AT potternergerm subthalamicandnigralneuronsaredifferentiallymodulatedduringparkinsoniangait |