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Subthalamic deep brain stimulation affects heading perception in Parkinson’s disease

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Abstract

Parkinson’s disease (PD) presents with visuospatial impairment and falls. It is critical to understand how subthalamic deep brain stimulation (STN DBS) modulates visuospatial perception. We hypothesized that DBS has different effects on visual and vestibular perception of linear motion (heading), a critical aspect of visuospatial navigation; and such effects are specific to modulated STN location. Two-alternative forced-choice experiments were performed in 14 PD patients with bilateral STN DBS and 19 age-matched healthy controls (HC) during passive en bloc linear motion and 3D optic-flow in immersive virtual reality measured vestibular and visual heading. Objective measure of perception with Weibull psychometric function revealed that PD has significantly lower accuracy [L: 60.71 (17.86)%, R: 74.82 (17.44)%] and higher thresholds [L: 16.68 (12.83), R: 10.09 (7.35)] during vestibular task in both directions compared to HC (p < 0.05). DBS significantly improved vestibular discrimination accuracy [81.40 (14.36)%] and threshold [4.12 (5.87), p < 0.05] in the rightward direction. There were no DBS effects on the slopes of vestibular psychometric curves. Visual heading perception was better than vestibular and it was comparable to HC. There was no significant effect of DBS on visual heading response accuracy or discrimination threshold (p > 0.05). Patient-specific DBS models revealed an association between change in vestibular heading perception and the modulation of the dorsal STN. In summary, DBS may have different effects on vestibular and visual heading perception in PD. These effects may manifest via dorsal STN putatively by its effects on the cerebellum.

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Acknowledgements

This work was supported by American Academy of Neurology Career Award (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 Fund). Dr. Shaikh has Penni and Stephen Weinberg Research Chair in Brain Health.

Funding

This work was supported by American Academy of Neurology Career Award (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). 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, Angela M. Noecker, Palak Gupta, Sarah Ozinga, Cameron C. McIntyre & 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, Mark F. Walker & Aasef G. Shaikh

  3. Department of Clinical Medicine-Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmark

    Mikkel Petersen

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

    Mark F. Walker, Camilla Kilbane & Aasef G. Shaikh

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

    Camilla Kilbane & Aasef G. Shaikh

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  1. Sinem Balta Beylergil
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  2. Angela M. Noecker
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  4. Palak Gupta
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Contributions

SBB: collected data, conceptualized analysis, performed analysis, and written and edited manuscript; AN: performed analysis and edited manuscript; CCM: performed analysis and edited manuscript; MP: performed analysis and edited manuscript; PG: collected data and edited manuscript; CK: collected data and edited manuscript; SO: conceptualized analysis, performed analysis, and edited manuscript; MW: conceptualized analysis and project, and edited manuscript; AGS: conceptualized project, analysis, collected data, performed analysis, and written and edited manuscript.

Corresponding author

Correspondence to Aasef G. Shaikh.

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Conflicts of interest

CCM is paid consultant for Boston Scientific Neuromodulation. CK has received honoraria from Medtronic Inc to serve as an advisor.

Data and code availability

Deidentified data and software codes will be made available to the interested party after preparing appropriate institutional agreements and approvals.

Ethics approval

Institutional Review Boards at Cleveland VA Medical Center and University Hospitals Cleveland Medical Center approved this study.

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The subjects signed informed consent form prior to participating in the study.

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Authors consented to publish their work. Patients consented to publish their deidentified data.

Supplementary Information

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415_2021_10616_MOESM1_ESM.tiff

Supplemental Fig. 1. Individual Weibull psychometric curves of HC for vestibular (solid line) and visual heading (dotted line) in the leftward (left half of the plot) and rightward heading direction (right half of the plot). Filled and open circles represent the subject’s percent correct responses in the vestibular and visual heading task, respectively. 75% threshold value, psychometric slope, as well as the goodness-of-fit (R2) value of each individual’s Weibull psychometric function are denoted and for each modality and heading direction (TIFF 5043 KB)

415_2021_10616_MOESM2_ESM.tiff

Supplemental Fig. 2. Individual Weibull psychometric curves of PD for vestibular (solid line) and visual heading (dotted line) in the leftward (left half of the plot) and rightward heading direction (right half of the plot). Psychometric curves in DBS-ON (red) and DBS-OFF (navy) conditions are plotted with average HC curves (black). Filled and open circles represent the subject’s percent correct responses in the vestibular and visual heading task, respectively. Dashed black horizontal line designates the 75% accuracy level. 75% threshold value, psychometric slope, as well as the goodness-of-fit (R2) value of each individual’s Weibull psychometric function are denoted and for each modality, DBS condition and heading direction (TIFF 3834 KB)

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Beylergil, S.B., Noecker, A.M., Petersen, M. et al. Subthalamic deep brain stimulation affects heading perception in Parkinson’s disease. J Neurol 269, 253–268 (2022). https://doi.org/10.1007/s00415-021-10616-4

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