Brain activation underlying turning in Parkinson's disease patients with and without freezing of gait: a virtual reality fMRI study

Moran Gilat; James M. Shine; Courtney C. Walton; Claire O'Callaghan; Julie M. Hall; Simon J. G. Lewis

doi:10.1038/npjparkd.2015.20

Brain activation underlying turning in Parkinson's disease patients with and without freezing of gait: a virtual reality fMRI study

Moran Gilat, James M. Shine, Courtney C. Walton, Claire O'Callaghan, Julie M. Hall, Simon J. G. Lewis^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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Abstract

BACKGROUND: Freezing of gait is a debilitating symptom affecting many patients with Parkinson's disease (PD), causing severe immobility and decreased quality of life. Turning is known to be the most common trigger for freezing and also causes the highest rates of falls. However, the pathophysiological basis for these effects is not well understood. METHODS: This study used a virtual reality paradigm in combination with functional magnetic resonance imaging to explore the neural correlates underlying turning in 17 PD patients with freezing of gait (FOG) and 10 PD patients without FOG while off their dopaminergic medication. Participants used foot pedals to navigate a virtual environment, which allowed for blood oxygen level-dependent (BOLD) responses and footstep latencies to be compared between periods of straight "walking" and periods of turning through 90°. BOLD data were then analyzed using a mixed effects analysis. RESULTS: Within group similarities revealed that overall, PD patients with freezing relied heavily on cortical control to enable effective stepping with increased visual cortex activation during turning. Between groups differences showed that when turning, patients with freezing preferentially activated inferior frontal regions that have been implicated in the recruitment of a putative stopping network. In addition, freezers failed to activate premotor and superior parietal cortices. Finally, increased task-based functional connectivity was found in subcortical regions associated with gait and stopping within the freezers group during turning. CONCLUSIONS: These findings suggest that an increased propensity towards stopping in combination with reduced sensorimotor integration may underlie the neurobiology of freezing of gait during turning.

Original language	English
Article number	15020
Pages (from-to)	1-9
Number of pages	9
Journal	Parkinson's Disease
Volume	1
DOIs	https://doi.org/10.1038/npjparkd.2015.20
Publication status	Published - 2015
Externally published	Yes

Bibliographical note

Copyright 2015 Parkinson's Disease Foundation/Macmillan Publishers Limited. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

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Publisher version (open access)Final published version, 1.2 MBLicence: CC BY

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title = "Brain activation underlying turning in Parkinson's disease patients with and without freezing of gait: a virtual reality fMRI study",

abstract = "BACKGROUND: Freezing of gait is a debilitating symptom affecting many patients with Parkinson's disease (PD), causing severe immobility and decreased quality of life. Turning is known to be the most common trigger for freezing and also causes the highest rates of falls. However, the pathophysiological basis for these effects is not well understood. METHODS: This study used a virtual reality paradigm in combination with functional magnetic resonance imaging to explore the neural correlates underlying turning in 17 PD patients with freezing of gait (FOG) and 10 PD patients without FOG while off their dopaminergic medication. Participants used foot pedals to navigate a virtual environment, which allowed for blood oxygen level-dependent (BOLD) responses and footstep latencies to be compared between periods of straight {"}walking{"} and periods of turning through 90°. BOLD data were then analyzed using a mixed effects analysis. RESULTS: Within group similarities revealed that overall, PD patients with freezing relied heavily on cortical control to enable effective stepping with increased visual cortex activation during turning. Between groups differences showed that when turning, patients with freezing preferentially activated inferior frontal regions that have been implicated in the recruitment of a putative stopping network. In addition, freezers failed to activate premotor and superior parietal cortices. Finally, increased task-based functional connectivity was found in subcortical regions associated with gait and stopping within the freezers group during turning. CONCLUSIONS: These findings suggest that an increased propensity towards stopping in combination with reduced sensorimotor integration may underlie the neurobiology of freezing of gait during turning.",

author = "Moran Gilat and Shine, {James M.} and Walton, {Courtney C.} and Claire O'Callaghan and Hall, {Julie M.} and Lewis, {Simon J. G.}",

note = "Copyright 2015 Parkinson's Disease Foundation/Macmillan Publishers Limited. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.",

year = "2015",

doi = "10.1038/npjparkd.2015.20",

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AU - Gilat, Moran

AU - Shine, James M.

AU - Walton, Courtney C.

AU - O'Callaghan, Claire

AU - Hall, Julie M.

AU - Lewis, Simon J. G.

N1 - Copyright 2015 Parkinson's Disease Foundation/Macmillan Publishers Limited. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

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Y1 - 2015

N2 - BACKGROUND: Freezing of gait is a debilitating symptom affecting many patients with Parkinson's disease (PD), causing severe immobility and decreased quality of life. Turning is known to be the most common trigger for freezing and also causes the highest rates of falls. However, the pathophysiological basis for these effects is not well understood. METHODS: This study used a virtual reality paradigm in combination with functional magnetic resonance imaging to explore the neural correlates underlying turning in 17 PD patients with freezing of gait (FOG) and 10 PD patients without FOG while off their dopaminergic medication. Participants used foot pedals to navigate a virtual environment, which allowed for blood oxygen level-dependent (BOLD) responses and footstep latencies to be compared between periods of straight "walking" and periods of turning through 90°. BOLD data were then analyzed using a mixed effects analysis. RESULTS: Within group similarities revealed that overall, PD patients with freezing relied heavily on cortical control to enable effective stepping with increased visual cortex activation during turning. Between groups differences showed that when turning, patients with freezing preferentially activated inferior frontal regions that have been implicated in the recruitment of a putative stopping network. In addition, freezers failed to activate premotor and superior parietal cortices. Finally, increased task-based functional connectivity was found in subcortical regions associated with gait and stopping within the freezers group during turning. CONCLUSIONS: These findings suggest that an increased propensity towards stopping in combination with reduced sensorimotor integration may underlie the neurobiology of freezing of gait during turning.

AB - BACKGROUND: Freezing of gait is a debilitating symptom affecting many patients with Parkinson's disease (PD), causing severe immobility and decreased quality of life. Turning is known to be the most common trigger for freezing and also causes the highest rates of falls. However, the pathophysiological basis for these effects is not well understood. METHODS: This study used a virtual reality paradigm in combination with functional magnetic resonance imaging to explore the neural correlates underlying turning in 17 PD patients with freezing of gait (FOG) and 10 PD patients without FOG while off their dopaminergic medication. Participants used foot pedals to navigate a virtual environment, which allowed for blood oxygen level-dependent (BOLD) responses and footstep latencies to be compared between periods of straight "walking" and periods of turning through 90°. BOLD data were then analyzed using a mixed effects analysis. RESULTS: Within group similarities revealed that overall, PD patients with freezing relied heavily on cortical control to enable effective stepping with increased visual cortex activation during turning. Between groups differences showed that when turning, patients with freezing preferentially activated inferior frontal regions that have been implicated in the recruitment of a putative stopping network. In addition, freezers failed to activate premotor and superior parietal cortices. Finally, increased task-based functional connectivity was found in subcortical regions associated with gait and stopping within the freezers group during turning. CONCLUSIONS: These findings suggest that an increased propensity towards stopping in combination with reduced sensorimotor integration may underlie the neurobiology of freezing of gait during turning.

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Brain activation underlying turning in Parkinson's disease patients with and without freezing of gait: a virtual reality fMRI study

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