Visual self-motion cues are impaired in Parkinson’s disease yet over-weighted during visual-vestibular integration

Abstract

Background: Parkinson's disease (PD) is prototypically a movement disorder.Although perceptual and motor functions are interdependent, much less is known about perceptual dysfunction in PD. Perceptual deficits can impact activities of daily living, and contribute to motor symptoms, but might go unnoticed if not tested directly. Posture, gait and balance, affected in PD, rely on veridical perception of one's own motion in space. Yet it is unknown whether self-motion perception is impaired in PD. Objectives:To test self-motion perception in PD, separately for visual and vestibular cues (unisensory), and multisensory integration thereof.Methods: Participants (19 early stage PD, 23 age-matched and 20 young adult controls) experienced vestibular (motion platform), visual (optic flow), and combined visual-vestibular self-motion stimuli, and discriminated whether the stimulus headings were rightward or leftward of straight ahead. PD participants and age-matched controls were tested on two visits (PD on and off medication).Results: PD participants had significantly impaired visual self-motion perception, both on and off medication. This deficit correlated significantly with clinical disease severity. By contrast, their vestibular performance was unimpaired. Remarkably, despite impaired visual self-motion perception, PD participants significantly overweighted visual cues during multisensory (visual-vestibular) integration. Conclusions:Self-motion perception is affected already in early stage PD, specifically by impaired visual (vs. vestibular) function, and by suboptimal visualvestibular integration. This may contribute to impaired balance and gait control. Future investigation into this connection might open up new avenues for alternativetherapies to better treat these symptoms. Furthermore, these results may also impact early PD diagnosis and subtyping.

Self‐motion perception in Parkinson's disease

“…Since responses are categorical (two‐alternative forced choice) and not graded motor responses, the resulting psychometric performance better isolates perceptual function. Recently, our group and another group, both tested vestibular heading discrimination in PD using this same method, but finding opposite results—Beylergil, Ozinga, Walker, McIntyre, and Shaikh (2019) found increased vestibular thresholds in PD, while we found no vestibular impairment (Yakubovich et al, in press). Our cohort were relatively early‐stage PD, while the other cohort were more advanced (with deep brain stimulation).…”

“…Yet, to conclude this, an experiment that measures unisensory reliabilities and multisensory integration weights within the Bayesian framework is required (taking care that measurements of unisensory function are indeed representative, otherwise predictions may be off, Shalom & Zaidel, 2018). In our recent study of heading discrimination (Yakubovich et al, in press), we indeed found visual overweighting in PD when comparing their measured visual and vestibular integration weights to the Bayesian predictions. Thus, patients with PD may have a specific (and perhaps unique) multisensory integration impairment.…”

“…sensorimotor) deficit. In a recent study by our group, we used categorical responses to specifically test perception of self‐motion and found impaired visual self‐motion perception in PD (Yakubovich et al, in press).…”

“…Accordingly, self‐motion perception in PD is probably compromised by ineffective integration of somatosensory information. Furthermore, impaired integration of vestibular signals in PD (Bertolini et al, 2015; Reichert et al, 1982; Vitale et al, 2011; Yakubovich et al, in press) may contribute to suboptimal self‐motion perception. Together these can have detrimental effects on motor function, including gait and balance.…”