Reaching to proprioceptively defined targets in Parkinson’s disease: Effects of deep brain stimulation therapy

•Parkinson’s patients show multijoint proprioceptive deficits.•Deep brain stimulation (DBS) of the STN has mixed effects on proprioception.•STN DBS improves the accuracy of limb localization in 3D space.•STN DBS increases variability (reduces precision) in limb localization. Deep brain stimulation o...

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Published inNeuroscience Vol. 244; pp. 99 - 112
Main Authors Lee, D., Henriques, D.Y., Snider, J., Song, D., Poizner, H.
Format Journal Article
LanguageEnglish
Published Amsterdam Elsevier Ltd 06.08.2013
Elsevier
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Online AccessGet full text
ISSN0306-4522
1873-7544
1873-7544
DOI10.1016/j.neuroscience.2013.04.009

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Abstract •Parkinson’s patients show multijoint proprioceptive deficits.•Deep brain stimulation (DBS) of the STN has mixed effects on proprioception.•STN DBS improves the accuracy of limb localization in 3D space.•STN DBS increases variability (reduces precision) in limb localization. Deep brain stimulation of the subthalamic nucleus (STN DBS) provides a unique window into human brain function since it can reversibly alter the functioning of specific brain circuits. Basal ganglia–cortical circuits are thought to be excessively noisy in patients with Parkinson’s disease (PD), based in part on the lack of specificity of proprioceptive signals in basal ganglia–thalamic–cortical circuits in monkey models of the disease. PD patients are known to have deficits in proprioception, but the effects are often subtle, with paradigms typically restricted to one or two joint movements in a plane. Moreover, the effects of STN DBS on proprioception are virtually unexplored. We tested the following hypotheses: first, that PD patients will show substantial deficits in unconstrained, multi-joint proprioception, and, second, that STN DBS will improve multi-joint proprioception. Twelve PD patients with bilaterally implanted electrodes in the subthalamic nucleus and 12 age-matched healthy subjects were asked to position the left hand at a location that was proprioceptively defined in 3D space with the right hand. In a second condition, subjects were provided visual feedback during the task so that they were not forced to rely on proprioception. Overall, with STN DBS switched off, PD patients showed significantly larger proprioceptive localization errors, and greater variability in endpoint localizations than the control subjects. Visual feedback partially normalized PD performance, and demonstrated that the errors in proprioceptive localization were not simply due to a difficulty in executing the movements or in remembering target locations. Switching STN DBS on significantly reduced localization errors from those of control subjects when patients moved without visual feedback relative to when they moved with visual feedback (when proprioception was not required). However, this reduction in localization errors without vision came at the cost of increased localization variability.
AbstractList Deep brain stimulation of the subthalamic nucleus (STN DBS) provides a unique window into human brain function since it can reversibly alter the functioning of specific brain circuits. Basal ganglia–cortical circuits are thought to be excessively noisy in patients with Parkinson’s disease (PD), based in part on the lack of specificity of proprioceptive signals in basal ganglia–thalamic–cortical circuits in monkey models of the disease. PD patients are known to have deficits in proprioception, but the effects are often subtle, with paradigms typically restricted to one or two joint movements in a plane. Moreover, the effects of STN DBS on proprioception are virtually unexplored. We tested the following hypotheses: first, that PD patients will show substantial deficits in unconstrained, multi-joint proprioception, and, second, that STN DBS will improve multi-joint proprioception. Twelve PD patients with bilaterally implanted electrodes in the subthalamic nucleus and 12 age-matched healthy subjects were asked to position the left hand at a location that was proprioceptively defined in 3D space with the right hand. In a second condition, subjects were provided visual feedback during the task so that they were not forced to rely on proprioception. Overall, with STN DBS switched off, PD patients showed significantly larger proprioceptive localization errors, and greater variability in endpoint localizations than the control subjects. Visual feedback partially normalized PD performance, and demonstrated that the errors in proprioceptive localization were not simply due to a difficulty in executing the movements or in remembering target locations. Switching STN DBS on significantly reduced localization errors from those of control subjects when patients moved without visual feedback relative to when they moved with visual feedback (when proprioception was not required). However, this reduction in localization errors without vision came at the cost of increased localization variability.
•Parkinson’s patients show multijoint proprioceptive deficits.•Deep brain stimulation (DBS) of the STN has mixed effects on proprioception.•STN DBS improves the accuracy of limb localization in 3D space.•STN DBS increases variability (reduces precision) in limb localization. Deep brain stimulation of the subthalamic nucleus (STN DBS) provides a unique window into human brain function since it can reversibly alter the functioning of specific brain circuits. Basal ganglia–cortical circuits are thought to be excessively noisy in patients with Parkinson’s disease (PD), based in part on the lack of specificity of proprioceptive signals in basal ganglia–thalamic–cortical circuits in monkey models of the disease. PD patients are known to have deficits in proprioception, but the effects are often subtle, with paradigms typically restricted to one or two joint movements in a plane. Moreover, the effects of STN DBS on proprioception are virtually unexplored. We tested the following hypotheses: first, that PD patients will show substantial deficits in unconstrained, multi-joint proprioception, and, second, that STN DBS will improve multi-joint proprioception. Twelve PD patients with bilaterally implanted electrodes in the subthalamic nucleus and 12 age-matched healthy subjects were asked to position the left hand at a location that was proprioceptively defined in 3D space with the right hand. In a second condition, subjects were provided visual feedback during the task so that they were not forced to rely on proprioception. Overall, with STN DBS switched off, PD patients showed significantly larger proprioceptive localization errors, and greater variability in endpoint localizations than the control subjects. Visual feedback partially normalized PD performance, and demonstrated that the errors in proprioceptive localization were not simply due to a difficulty in executing the movements or in remembering target locations. Switching STN DBS on significantly reduced localization errors from those of control subjects when patients moved without visual feedback relative to when they moved with visual feedback (when proprioception was not required). However, this reduction in localization errors without vision came at the cost of increased localization variability.
Highlights • Parkinson’s patients show multijoint proprioceptive deficits. • Deep brain stimulation (DBS) of the STN has mixed effects on proprioception. • STN DBS improves the accuracy of limb localization in 3D space. • STN DBS increases variability (reduces precision) in limb localization.
Deep brain stimulation of the subthalamic nucleus (STN DBS) provides a unique window into human brain function since it can reversibly alter the functioning of specific brain circuits. Basal ganglia-cortical circuits are thought to be excessively noisy in patients with Parkinson's disease (PD), based in part on the lack of specificity of proprioceptive signals in basal ganglia-thalamic-cortical circuits in monkey models of the disease. PD patients are known to have deficits in proprioception, but the effects are often subtle, with paradigms typically restricted to one or two joint movements in a plane. Moreover, the effects of STN DBS on proprioception are virtually unexplored. We tested the following hypotheses: first, that PD patients will show substantial deficits in unconstrained, multi-joint proprioception, and, second, that STN DBS will improve multi-joint proprioception. Twelve PD patients with bilaterally implanted electrodes in the subthalamic nucleus and 12 age-matched healthy subjects were asked to position the left hand at a location that was proprioceptively defined in 3D space with the right hand. In a second condition, subjects were provided visual feedback during the task so that they were not forced to rely on proprioception. Overall, with STN DBS switched off, PD patients showed significantly larger proprioceptive localization errors, and greater variability in endpoint localizations than the control subjects. Visual feedback partially normalized PD performance, and demonstrated that the errors in proprioceptive localization were not simply due to a difficulty in executing the movements or in remembering target locations. Switching STN DBS on significantly reduced localization errors from those of control subjects when patients moved without visual feedback relative to when they moved with visual feedback (when proprioception was not required). However, this reduction in localization errors without vision came at the cost of increased localization variability.Deep brain stimulation of the subthalamic nucleus (STN DBS) provides a unique window into human brain function since it can reversibly alter the functioning of specific brain circuits. Basal ganglia-cortical circuits are thought to be excessively noisy in patients with Parkinson's disease (PD), based in part on the lack of specificity of proprioceptive signals in basal ganglia-thalamic-cortical circuits in monkey models of the disease. PD patients are known to have deficits in proprioception, but the effects are often subtle, with paradigms typically restricted to one or two joint movements in a plane. Moreover, the effects of STN DBS on proprioception are virtually unexplored. We tested the following hypotheses: first, that PD patients will show substantial deficits in unconstrained, multi-joint proprioception, and, second, that STN DBS will improve multi-joint proprioception. Twelve PD patients with bilaterally implanted electrodes in the subthalamic nucleus and 12 age-matched healthy subjects were asked to position the left hand at a location that was proprioceptively defined in 3D space with the right hand. In a second condition, subjects were provided visual feedback during the task so that they were not forced to rely on proprioception. Overall, with STN DBS switched off, PD patients showed significantly larger proprioceptive localization errors, and greater variability in endpoint localizations than the control subjects. Visual feedback partially normalized PD performance, and demonstrated that the errors in proprioceptive localization were not simply due to a difficulty in executing the movements or in remembering target locations. Switching STN DBS on significantly reduced localization errors from those of control subjects when patients moved without visual feedback relative to when they moved with visual feedback (when proprioception was not required). However, this reduction in localization errors without vision came at the cost of increased localization variability.
Author Song, D.
Lee, D.
Henriques, D.Y.
Snider, J.
Poizner, H.
AuthorAffiliation a Institute for Neural Computation, University of California, San Diego, CA, United States
b School of Kinesiology & Health Science Centre for Vision Research, York University, Toronto, Canada
d Graduate Program in Neurosciences, University of California, San Diego, CA, United States
c Department of Neurosciences, University of California, San Diego, CA, United States
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Keywords GPi
DBS
PD
subthalamic nucleus
UPDRS
STN
proprioception
human
deep brain stimulation
Parkinson’s disease
United Parkinson’s Disease Rating Scale
internal (medial) segment of the globus pallidus
Human
Nervous system diseases
Parkinson's disease
Proprioception
Deep brain stimulation
Central nervous system
Parkinson disease
Encephalon
Cerebral disorder
Central nervous system disease
Degenerative disease
Subthalamic nucleus
Extrapyramidal syndrome
Language English
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CC BY 4.0
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Present address: Department of Electrical Engineering, Korea Advanced Institute of Science and Technology, Daejeon, Republic of Korea. Center for Integrated Smart Sensors, Daejoen, Republic of Korea.
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Snippet •Parkinson’s patients show multijoint proprioceptive deficits.•Deep brain stimulation (DBS) of the STN has mixed effects on proprioception.•STN DBS improves...
Highlights • Parkinson’s patients show multijoint proprioceptive deficits. • Deep brain stimulation (DBS) of the STN has mixed effects on proprioception. • STN...
Deep brain stimulation of the subthalamic nucleus (STN DBS) provides a unique window into human brain function since it can reversibly alter the functioning of...
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SubjectTerms Aged
Biological and medical sciences
Deep Brain Stimulation
Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases
Feedback, Sensory - physiology
Female
human
Humans
Male
Medical sciences
Nervous system (semeiology, syndromes)
Nervous system as a whole
Neurology
Parkinson Disease - complications
Parkinson Disease - therapy
Parkinson’s disease
proprioception
Psychomotor Performance - physiology
Somatosensory Disorders - complications
Somatosensory Disorders - therapy
subthalamic nucleus
Subthalamic Nucleus - physiology
Title Reaching to proprioceptively defined targets in Parkinson’s disease: Effects of deep brain stimulation therapy
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https://www.clinicalkey.es/playcontent/1-s2.0-S0306452213003278
https://dx.doi.org/10.1016/j.neuroscience.2013.04.009
https://www.ncbi.nlm.nih.gov/pubmed/23590906
https://www.proquest.com/docview/1357496937
https://pubmed.ncbi.nlm.nih.gov/PMC3780593
Volume 244
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