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Does visuospatial motion perception correlate with coexisting movement disorders in Parkinson’s disease?

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Abstract

Postural instability and balance impairment are common in Parkinson's disease (PD). Multiple factors, such as increased tone, bradykinesia, freezing of gait, posture, axial stiffness, and involuntary appendicular movements, can affect balance. The recent studies found that PD patients have abnormal perception of self-motion in vestibular domain. We asked whether measures of balance function, such as perception of one’s motion, correlate with specific movement disorders seen in PD. Moving retinal image or self-motion in space triggers the perception of self-motion. We measured one’s linear motion (heading) perception when subjects were moved en bloc using a moving platform (vestibular heading). Similar motion perception was generated in the visual domain (visual heading) by having the subjects view a 3D optical flow with immersive virtual reality goggles. During both tasks, the subjects reported the motion direction in the two-alternative-forced-choice paradigm. The accuracy of perceived motion direction was calculated from the responses fitted to the psychometric function curves to estimate how accurately and precisely the subjects can perceive rightward versus leftward motion (i.e., threshold and slope). Response accuracies and psychometric parameters were correlated with the disease duration, disease severity (total Unified Parkinson’s Disease Rating Scale-III, UPDRS-III), and tremor, rigidity, axial, gait/posture components of UPRDS-III. We also correlated heading perception with the number of falls and subjective assessment of balance confidence using the Activities-Specific Balance Component (ABC) Scale. Accuracy, threshold, and sensitivity of vestibular heading perception significantly correlated with the disease duration and severity, particularly the tremor. Correlations were stronger for leftward heading perception in the vestibular domain. The visual heading perception was correlated with ABC Scale, especially with its items concerning optic-flow processing. There was asymmetry in leftward versus rightward vestibular heading perception. The level of asymmetry correlated with the axial component of UPDRS-III. Differences in the clinical parameters that correlate with visual versus vestibular heading perception suggest that two heading perception processes have different mechanistic underpinnings. The correlation of discordance between vestibular and visual heading perception with disease severity and duration suggests that visual function can be utilized for balance rehab in PD patients.

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Acknowledgements

Grants from The American Academy of Neurology (Shaikh), American Parkinson’s Disease Association George C Cotzias Memorial Fellowship (Shaikh), Dystonia Medical Research Foundation Research (Shaikh), and Department of Veterans Affairs (I01 CX002086-01A2) and philanthropic funds to the Department of Neurology at University Hospitals (The Allan Woll Fund and The Fox Fund) supported this research. Shaikh holds Penni and Steven Weinberg Chair in Brain Health. The authors thank Cameron McIntyre, PhD, Sarah Ozinga, PhD, and Mark Walker, MD for their support.

Funding

This work was supported by American Academy of Neurology Career Award (Shaikh), Department of Veterans Affairs Clinical Science R & D Merit Review Grant (I01 CX002086-01A2) (Shaikh), American Parkinson’s Disease Association George C Cotzias Memorial Fellowship (Shaikh), Dystonia Medical Research Foundation Research Grant (Shaikh), and philanthropic funds to the Department of Neurology at University Hospitals (The Allan Woll Fund and The Fox Family Fund). Dr.Shaikh has Penni and Stephen Weinberg Chair in Brain Health.

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Authors and Affiliations

  1. Department of Biomedical Engineering, Case Western Reserve University, Cleveland, OH, USA

    Sinem Balta Beylergil, Palak Gupta & Aasef G. Shaikh

  2. National VA Parkinson Consortium Center, Neurology Service, Daroff-Dell’Osso Ocular Motility and Vestibular Laboratory, Louis Stokes Cleveland VA Medical Center, Cleveland, OH, USA

    Sinem Balta Beylergil, Palak Gupta & Aasef G. Shaikh

  3. Department of Neurology, Case Western Reserve University, 11100 Euclid Avenue, Cleveland, OH, 44110, USA

    Mohamed ElKasaby, Camilla Kilbane & Aasef G. Shaikh

  4. Movement Disorders Center, Neurological Institute, University Hospitals, Cleveland, OH, USA

    Mohamed ElKasaby, Camilla Kilbane & Aasef G. Shaikh

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  1. Sinem Balta Beylergil
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Contributions

SBB: collected data, conceptualized analysis, performed analysis, written and edited manuscript; PG: collected data, edited manuscript; CK and ME: collected data, edited manuscript; AGS: conceptualized project, analysis, collected data, performed analysis, written and edited manuscript.

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Correspondence to Aasef G. Shaikh.

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CK has received honoraria from Medtronic Inc to serve as an advisor.

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Beylergil, S.B., Gupta, P., ElKasaby, M. et al. Does visuospatial motion perception correlate with coexisting movement disorders in Parkinson’s disease?. J Neurol 269, 2179–2192 (2022). https://doi.org/10.1007/s00415-021-10804-2

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