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Internally Guided Lower Limb Movement Recruits Compensatory Cerebellar Activity in People With Parkinson's Disease

Background: Externally guided (EG) and internally guided (IG) movements are postulated to recruit two parallel neural circuits, in which motor cortical neurons interact with either the cerebellum or striatum via distinct thalamic nuclei. Research suggests EG movements rely more heavily on the cerebe...

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Autores principales: Drucker, Jonathan H., Sathian, K., Crosson, Bruce, Krishnamurthy, Venkatagiri, McGregor, Keith M., Bozzorg, Ariyana, Gopinath, Kaundinya, Krishnamurthy, Lisa C., Wolf, Steven L., Hart, Ariel R., Evatt, Marian, Corcos, Daniel M., Hackney, Madeleine E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6566131/
https://www.ncbi.nlm.nih.gov/pubmed/31231297
http://dx.doi.org/10.3389/fneur.2019.00537
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author Drucker, Jonathan H.
Sathian, K.
Crosson, Bruce
Krishnamurthy, Venkatagiri
McGregor, Keith M.
Bozzorg, Ariyana
Gopinath, Kaundinya
Krishnamurthy, Lisa C.
Wolf, Steven L.
Hart, Ariel R.
Evatt, Marian
Corcos, Daniel M.
Hackney, Madeleine E.
author_facet Drucker, Jonathan H.
Sathian, K.
Crosson, Bruce
Krishnamurthy, Venkatagiri
McGregor, Keith M.
Bozzorg, Ariyana
Gopinath, Kaundinya
Krishnamurthy, Lisa C.
Wolf, Steven L.
Hart, Ariel R.
Evatt, Marian
Corcos, Daniel M.
Hackney, Madeleine E.
author_sort Drucker, Jonathan H.
collection PubMed
description Background: Externally guided (EG) and internally guided (IG) movements are postulated to recruit two parallel neural circuits, in which motor cortical neurons interact with either the cerebellum or striatum via distinct thalamic nuclei. Research suggests EG movements rely more heavily on the cerebello-thalamo-cortical circuit, whereas IG movements rely more on the striato-pallido-thalamo-cortical circuit (1). Because Parkinson's (PD) involves striatal dysfunction, individuals with PD have difficulty generating IG movements (2). Objectives: Determine whether individuals with PD would employ a compensatory mechanism favoring the cerebellum over the striatum during IG lower limb movements. Methods: 22 older adults with mild-moderate PD, who had abstained at least 12 h from anti-PD medications, and 19 age-matched controls performed EG and IG rhythmic foot-tapping during functional magnetic resonance imaging. Participants with PD tapped with their right (more affected) foot. External guidance was paced by a researcher tapping participants' ipsilateral 3rd metacarpal in a pattern with 0.5 to 1 s intervals, while internal guidance was based on pre-scan training in the same pattern. BOLD activation was compared between tasks (EG vs. IG) and groups (PD vs. control). Results: Both groups recruited the putamen and cerebellar regions. The PD group demonstrated less activation in the striatum and motor cortex than controls. A task (EG vs. IG) by group (PD vs. control) interaction was observed in the cerebellum with increased activation for the IG condition in the PD group. Conclusions: These findings support the hypothesized compensatory shift in which the dysfunctional striatum is assisted by the less affected cerebellum to accomplish IG lower limb movement in individuals with mild-moderate PD. These findings are of relevance for temporal gait dysfunction and freezing of gait problems frequently noted in many people with PD and may have implications for future therapeutic application.
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spelling pubmed-65661312019-06-21 Internally Guided Lower Limb Movement Recruits Compensatory Cerebellar Activity in People With Parkinson's Disease Drucker, Jonathan H. Sathian, K. Crosson, Bruce Krishnamurthy, Venkatagiri McGregor, Keith M. Bozzorg, Ariyana Gopinath, Kaundinya Krishnamurthy, Lisa C. Wolf, Steven L. Hart, Ariel R. Evatt, Marian Corcos, Daniel M. Hackney, Madeleine E. Front Neurol Neurology Background: Externally guided (EG) and internally guided (IG) movements are postulated to recruit two parallel neural circuits, in which motor cortical neurons interact with either the cerebellum or striatum via distinct thalamic nuclei. Research suggests EG movements rely more heavily on the cerebello-thalamo-cortical circuit, whereas IG movements rely more on the striato-pallido-thalamo-cortical circuit (1). Because Parkinson's (PD) involves striatal dysfunction, individuals with PD have difficulty generating IG movements (2). Objectives: Determine whether individuals with PD would employ a compensatory mechanism favoring the cerebellum over the striatum during IG lower limb movements. Methods: 22 older adults with mild-moderate PD, who had abstained at least 12 h from anti-PD medications, and 19 age-matched controls performed EG and IG rhythmic foot-tapping during functional magnetic resonance imaging. Participants with PD tapped with their right (more affected) foot. External guidance was paced by a researcher tapping participants' ipsilateral 3rd metacarpal in a pattern with 0.5 to 1 s intervals, while internal guidance was based on pre-scan training in the same pattern. BOLD activation was compared between tasks (EG vs. IG) and groups (PD vs. control). Results: Both groups recruited the putamen and cerebellar regions. The PD group demonstrated less activation in the striatum and motor cortex than controls. A task (EG vs. IG) by group (PD vs. control) interaction was observed in the cerebellum with increased activation for the IG condition in the PD group. Conclusions: These findings support the hypothesized compensatory shift in which the dysfunctional striatum is assisted by the less affected cerebellum to accomplish IG lower limb movement in individuals with mild-moderate PD. These findings are of relevance for temporal gait dysfunction and freezing of gait problems frequently noted in many people with PD and may have implications for future therapeutic application. Frontiers Media S.A. 2019-06-07 /pmc/articles/PMC6566131/ /pubmed/31231297 http://dx.doi.org/10.3389/fneur.2019.00537 Text en Copyright © 2019 Drucker, Sathian, Crosson, Krishnamurthy, McGregor, Bozzorg, Gopinath, Krishnamurthy, Wolf, Hart, Evatt, Corcos and Hackney. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Drucker, Jonathan H.
Sathian, K.
Crosson, Bruce
Krishnamurthy, Venkatagiri
McGregor, Keith M.
Bozzorg, Ariyana
Gopinath, Kaundinya
Krishnamurthy, Lisa C.
Wolf, Steven L.
Hart, Ariel R.
Evatt, Marian
Corcos, Daniel M.
Hackney, Madeleine E.
Internally Guided Lower Limb Movement Recruits Compensatory Cerebellar Activity in People With Parkinson's Disease
title Internally Guided Lower Limb Movement Recruits Compensatory Cerebellar Activity in People With Parkinson's Disease
title_full Internally Guided Lower Limb Movement Recruits Compensatory Cerebellar Activity in People With Parkinson's Disease
title_fullStr Internally Guided Lower Limb Movement Recruits Compensatory Cerebellar Activity in People With Parkinson's Disease
title_full_unstemmed Internally Guided Lower Limb Movement Recruits Compensatory Cerebellar Activity in People With Parkinson's Disease
title_short Internally Guided Lower Limb Movement Recruits Compensatory Cerebellar Activity in People With Parkinson's Disease
title_sort internally guided lower limb movement recruits compensatory cerebellar activity in people with parkinson's disease
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6566131/
https://www.ncbi.nlm.nih.gov/pubmed/31231297
http://dx.doi.org/10.3389/fneur.2019.00537
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