Vestibular Heading Perception in Parkinson's Disease Patients treated with Deep Brain Stimulation
Sinem Balta Beylergil1,2, Mark F Walker2,3, Sarah Ozinga1, Angela M Noecker1, Cameron C McIntyre1, and Aasef G. Shaikh2,3,4
1Department of Biomedical Engineering, Case Western Reserve University, Cleveland OH, 2Department of Neurology,VA Medical Center, Cleveland OH, 3Department of Neurology, Case Western Reserve University, Cleveland OH, 4Department of Neurology, University Hospitals, Cleveland OH
Background: Postural instability and gait dysfunction, which depend on reliable estimates of self-motion or heading relative to the surrounding environment, are frequent causes of falls in Parkinson’s Disease (PD). Heading perception relies on the integration of visual, vestibular, and proprioceptive information. In PD, the processing of proprioception is impaired, increasing the dependence on visual and vestibular modalities. While recent clinical investigations have emphasized deteriorated visuospatial function contributing to heading and gait instability in PD, much of this work was based solely on visual cues. The vestibular system is a powerful and independent source that provides valuable input to heading perception. Compared to the visual system, much less is known regarding the integrative process of vestibular information required for heading perception in PD. Moreover, modulation of the basal ganglia output using subthalamic deep brain stimulation (StnDBS) in PD can affect cerebellar excitability and thalamic drive, which have potential to influence the physiological mechanisms that calibrate heading perception.
Aims: This study aims to determine how the ability to perceive heading direction in the absence of visual cues is affected in PD. We also investigate the effect of StnDBS on vestibular heading perception. In this context, we aim to identify the brain pathways that influence the brainstem, cerebellar, thalamic, and cerebral cortex vestibular networks responsible for heading perception.
Methods: PD patients with bilateral StnDBS and age-matched healthy participants performed a two-alternative, forced-choice heading discrimination task, while they were seated in a padded chair mounted on the hexapod (MOOGTM, East Aurora, NY). Each trial comprised of a forward passive whole-body translation along linear horizontal trajectories 2.5°, 5°, 10°, 20°, 30° to the right or the left in complete darkness wearing blindfold. After each trial, subjects were asked to indicate whether the movement was rightward or leftward relative to straight-ahead. PD subjects performed the experiment twice, once in the absence and once in the presence of therapeutic electrical stimulation. Sensitivity of the vestibular system to subtle variations in heading direction and systematic errors in accuracy of responses were derived for each subject using a Gaussian psychometric function. Additionally, we used an academic DBS research tool, StimVision Software, to build patient-specific anatomical models of StnDBS and predict percentages of axonal pathways that were activated by StnDBS.
Results: Compared to healthy subjects, PD presented with the highest angular threshold to detect heading direction, and their perception of self-motion was less sensitive to the variations in heading direction. When the StnDBS was turned on, heading perception performance improved and reached a level comparable to the performance of the age-matched healthy control subjects. The anatomical model of the StnDBS revealed that up to 50% of cerebello-thalamic track fibers were stimulated by StnDBS.
Conclusion: Our results show that heading perception guided by vestibular information was deteriorated in PD. StnDBS seemed to be able to restore the impairment possibly by modulating the cerebello-thalamic pathway. These results confirm the potential of our study to provide valuable insight to vestibular system’s role in spatial navigation deficits in PD.