Abstract

Parkinson's disease (PD), best characterized by its classic motor symptoms, also manifests non-motor symptoms including perceptual impairments. Normal motor and perceptual brain functions interact continuously in an action-perception loop; hence, perceptual and motor dysfunction in PD are likely also intertwined. A vital skill in order to maintain balance, and to move around in the environment is the ability to perceive one's own motion in space (self-motion perception). Self-motion perception is a complex brain process, that requires the integration of information from visual (optic flow), vestibular (gravito-inertial), and somatosensory senses. Yet, not much is known about self-motion perception or multisensory integration in PD. In this review, we highlight the need to better study these important functions in PD. We review perceptual deficits in underlying functions required for adept self-motion perception (visual, vestibular and somatosensory, as well as multisensory integration) and address how these might affect self-motion perception and motor function in PD. We propose that dysfunction of central brain mechanisms, implicated in impaired visual, vestibular and somatosensory function, likely impact self-motion perception in PD. Recent evidence suggests that visual and multisensory integration mechanisms of self-motion perception are indeed impaired in PD. This can affect motor control, gait and balance. Future research is needed to better investigate this important topic. A better understanding of self-motion perception and multisensory integration in PD may aid diagnosis and subtyping and may open new avenues for novel therapies to treat debilitating motor symptoms, including gait and balance impairment, using sensory augmentation devices or sensory retraining.


Authors

Halperin, Orly;  Israeli-Korn, Simon;  Yakubovich, Sol;  Hassin-Baer, Sharon;  Zaidel, Adam

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  • pre-publication peer review (FINAL ROUND)
    Decision Letter
    2020/02/24

    24-Feb-2020

    EJN-2020-01-27031(BIBAGS).R1
    Self-Motion Perception in Parkinson's disease

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    Author Response
    2020/02/23

    Dear Editor Prof. Yoland Smith,
    Thank you for the exceptionally fast handling of the first round of reviews, and for the positive outcome. We have revised our manuscript in accordance with the minor suggestions raised by the reviewers. Please see our specific responses to the reviewers suggestions in the "Authors' Response to Reviewers" document. We have marked changes to the manuscript by underlining them.
    Yours sincerely,
    Orly Halperin, Simon Israeli-Korn, Sol Yakubovich, Sharon Hassin-Baer and Adam Zaidel



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  • pre-publication peer review (ROUND 1)
    Decision Letter
    2020/02/09

    09-Feb-2020

    Manuscript Number:EJN-2020-01-27031(BIBAGS)
    Self-Motion Perception in Parkinson's disease

    Dear Dr. Zaidel,

    Your manuscript was reviewed by two external reviewers and the process was handled by our Senior Editor, Professor Yoland Smith. Both reviewers considered that your review was well prepared, thorough and highly relevant to advance the field of PD research and clinical care. Please, address some of the minor suggestions they raised to improve the quality of this excellent review.

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    Reviews:

    Reviewer: 1

    Comments to the Author
    The authors have presented a comprehensive summary of perception deficits in Parkinson's disease. The writing is well done.

    Two recommendations that would potentially improve the work are:

    1. In the Introduction, the authors state that certain PD symptoms "respond poorly" to dopaminergic therapy. It would be helpful to be more precise with what they mean by this. Do they mean acute levodopa challenge, chronic levodopa therapy, or DBS? This type of language is quite common clinically but is prone to misinterpretation by basic neuroscientists unfamiliar with PD clinical management. A recent reference that may be relevant for demonstrating one method of measuring levodopa response (with its own limitations) is this recent work using an acute levodopa challenge:

    McKay JL, Goldstein FC, Sommerfeld B, Bernhard D, Perez Parra S, Factor SA, 2020. Freezing of Gait can persist after an acute levodopa challenge in Parkinson’s disease. npj Parkinson's disease 5: 25. https://doi.org/10.1038/s41531-019-0099-z.

    1. That vision is the strongest factor influencing self-motion perception in PD is a strong statement to make. It was recently shown (reference below) that PD patients also have impaired perception of body motion during translation paradigms in blindfolded conditions. This suggests that visual impairments may prevent visual compensation for proprioceptive deficits in self-motion. (This may be interesting to consider in light of the circumstances of falls in PD, which often occur at home in visually cluttered environments. So perhaps the causal pathway that leads to falls is that visual deficits or visual clutter could impair compensation for impaired self-motion perception.) This section could be improved by a sentence or two elaborating a more concrete example of the way in which they hypothesize impaired visual perception to cause impaired self-motion perception.

    Bong SM, McKay JL, Factor SA, Ting LH, 2019. Perception of whole-body motion during balance perturbations is impaired in Parkinson's disease and is associated with balance impairment. Gait and Posture 76:44-50.

    Reviewer: 2

    Comments to the Author
    In the manuscript titled "Self-Motion Perception in Parkinson's disease" Halperin et al. review the currently existing literature regarding visual, vestibular and somatosensory perceptual impairments in Parkinson's disease.

    The manuscript is thorough and well-written. The manuscript could be additionally improved by adding information regarding pathological evidences (alpha-synuclein accumulation / atrophy) for involvement of the relevant neuronal networks (other than basal ganglia networks).

    One minor typo: Opening sentence of the abstract - remove extra comma.


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    Decision letter by
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    Reviewer report
    2020/02/09

    In the manuscript titled "Self-Motion Perception in Parkinson's disease" Halperin et al. review the currently existing literature regarding visual, vestibular and somatosensory perceptual impairments in Parkinson's disease.

    The manuscript is thorough and well-written. The manuscript could be additionally improved by adding information regarding pathological evidences (alpha-synuclein accumulation / atrophy) for involvement of the relevant neuronal networks (other than basal ganglia networks).

    One minor typo: Opening sentence of the abstract - remove extra comma.

    Reviewed by
    Cite this review
    Reviewer report
    2020/02/03

    The authors have presented a comprehensive summary of perception deficits in Parkinson's disease. The writing is well done.

    Two recommendations that would potentially improve the work are:

    1. In the Introduction, the authors state that certain PD symptoms "respond poorly" to dopaminergic therapy. It would be helpful to be more precise with what they mean by this. Do they mean acute levodopa challenge, chronic levodopa therapy, or DBS? This type of language is quite common clinically but is prone to misinterpretation by basic neuroscientists unfamiliar with PD clinical management. A recent reference that may be relevant for demonstrating one method of measuring levodopa response (with its own limitations) is this recent work using an acute levodopa challenge:

    McKay JL, Goldstein FC, Sommerfeld B, Bernhard D, Perez Parra S, Factor SA, 2020. Freezing of Gait can persist after an acute levodopa challenge in Parkinson’s disease. npj Parkinson's disease 5: 25. https://doi.org/10.1038/s41531-019-0099-z.

    1. That vision is the strongest factor influencing self-motion perception in PD is a strong statement to make. It was recently shown (reference below) that PD patients also have impaired perception of body motion during translation paradigms in blindfolded conditions. This suggests that visual impairments may prevent visual compensation for proprioceptive deficits in self-motion. (This may be interesting to consider in light of the circumstances of falls in PD, which often occur at home in visually cluttered environments. So perhaps the causal pathway that leads to falls is that visual deficits or visual clutter could impair compensation for impaired self-motion perception.) This section could be improved by a sentence or two elaborating a more concrete example of the way in which they hypothesize impaired visual perception to cause impaired self-motion perception.

    Bong SM, McKay JL, Factor SA, Ting LH, 2019. Perception of whole-body motion during balance perturbations is impaired in Parkinson's disease and is associated with balance impairment. Gait and Posture 76:44-50.

    Reviewed by
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