Internally guided lower limb movement recruits compensatory cerebellar activity in people with Parkinson's disease

Jonathan H. Drucker, K. Sathian, Bruce Crosson, Venkatagiri Krishnamurthy, Keith M. McGregor, Ariyana Bozzorg, Kaundinya Gopinath, Lisa C. Krishnamurthy, Steven L. Wolf, Ariel R. Hart, Marian Evatt, Daniel M. Corcos, Madeleine E. Hackney

Research output: Contribution to journalArticle

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Abstract

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.

Original languageEnglish (US)
Article number537
JournalFrontiers in Neurology
Volume10
Issue numberJUN
DOIs
StatePublished - Jan 1 2019

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Cerebellum
Parkinson Disease
Lower Extremity
Gait
Foot
Corpus Striatum
Thalamic Nuclei
Metacarpal Bones
Putamen
Motor Cortex
Motor Neurons
Freezing
Research Personnel
Magnetic Resonance Imaging
Research
Therapeutics

All Science Journal Classification (ASJC) codes

  • Neurology
  • Clinical Neurology

Cite this

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. In: Frontiers in Neurology. 2019 ; Vol. 10, No. JUN.
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title = "Internally guided lower limb movement recruits compensatory cerebellar activity in people with Parkinson's disease",
abstract = "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.",
author = "Drucker, {Jonathan H.} and K. Sathian and Bruce Crosson and Venkatagiri Krishnamurthy and McGregor, {Keith M.} and Ariyana Bozzorg and Kaundinya Gopinath and Krishnamurthy, {Lisa C.} and Wolf, {Steven L.} and Hart, {Ariel R.} and Marian Evatt and Corcos, {Daniel M.} and Hackney, {Madeleine E.}",
year = "2019",
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doi = "10.3389/fneur.2019.00537",
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Drucker, JH, Sathian, K, Crosson, B, Krishnamurthy, V, McGregor, KM, Bozzorg, A, Gopinath, K, Krishnamurthy, LC, Wolf, SL, Hart, AR, Evatt, M, Corcos, DM & Hackney, ME 2019, 'Internally guided lower limb movement recruits compensatory cerebellar activity in people with Parkinson's disease', Frontiers in Neurology, vol. 10, no. JUN, 537. https://doi.org/10.3389/fneur.2019.00537

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.

In: Frontiers in Neurology, Vol. 10, No. JUN, 537, 01.01.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Internally guided lower limb movement recruits compensatory cerebellar activity in people with Parkinson's disease

AU - Drucker, Jonathan H.

AU - Sathian, K.

AU - Crosson, Bruce

AU - Krishnamurthy, Venkatagiri

AU - McGregor, Keith M.

AU - Bozzorg, Ariyana

AU - Gopinath, Kaundinya

AU - Krishnamurthy, Lisa C.

AU - Wolf, Steven L.

AU - Hart, Ariel R.

AU - Evatt, Marian

AU - Corcos, Daniel M.

AU - Hackney, Madeleine E.

PY - 2019/1/1

Y1 - 2019/1/1

N2 - 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.

AB - 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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