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

Abstract

Parkinson’s disease is prototypically a movement disorder. Although perceptual and motor functions are highly interdependent, much less is known about perceptual deficits in Parkinson’s disease, which are less observable by nature, and might go unnoticed if not tested directly. It is therefore imperative to seek and identify these, to fully understand the challenges facing patients with Parkinson’s disease. Also, perceptual deficits may be related to motor symptoms. Posture, gait and balance, affected in Parkinson’s disease, rely on veridical perception of one’s own motion (self-motion) in space. Yet it is not known whether self-motion perception is impaired in Parkinson’s disease. Using a well-established multisensory paradigm of heading discrimination (that has not been previously applied to Parkinson’s disease), we tested unisensory visual and vestibular self-motion perception, as well as multisensory integration of visual and vestibular cues, in 19 Parkinson’s disease, 23 healthy age-matched and 20 healthy young-adult participants. After experiencing vestibular (on a motion platform), visual (optic flow) or multisensory (combined visual–vestibular) self-motion stimuli at various headings, participants reported whether their perceived heading was to the right or left of straight ahead. Parkinson’s disease participants and age-matched controls were tested twice (Parkinson’s disease participants on and off medication). Parkinson’s disease participants demonstrated significantly impaired visual self-motion perception compared with age-matched controls on both visits, irrespective of medication status. Young controls performed slightly (but not significantly) better than age-matched controls and significantly better than the Parkinson’s disease group. The visual self-motion perception impairment in Parkinson’s disease correlated significantly with clinical disease severity. By contrast, vestibular performance was unimpaired in Parkinson’s disease. Remarkably, despite impaired visual self-motion perception, Parkinson’s disease participants significantly overweighted the visual cues during multisensory (visual–vestibular ) integration (compared with Bayesian predictions of optimal integration) and significantly more than controls. These findings indicate that self-motion perception in Parkinson’s disease is affected by impaired visual cues and by suboptimal visual–vestibular integration (overweighting of visual cues). Notably, vestibular self-motion perception was unimpaired. Thus, visual self-motion perception is specifically impaired in early-stage Parkinson’s disease. This can impact Parkinson’s disease diagnosis and subtyping. Overweighting of visual cues could reflect a general multisensory integration deficit in Parkinson’s disease, or specific overestimation of visual cue reliability. Finally, impaired self-motion perception in Parkinson’s disease may contribute to impaired balance and gait control. Future investigation into this connection might open up new avenues of alternative therapies to better treat these difficult symptoms.

Overconfidence in visual perception in Parkinson’s disease

“…However, despite similar psychophysical performance, PD patients were significantly overconfident in their perceptual decisions. This suggests that PD patients overestimate the reliability of their visual cues, which might explain recent findings of visual overweighting during multisensory integration (Yakubovich et al, 2020), and descriptions of increased dependence on vision (Cooke et al, 1978;Bronstein et al, 1990;Azulay et al, 1999Azulay et al, , 2002Almeida and Lebold, 2010;Cowie et al, 2010) in PD. White et al (2016) recently found that PD patients overestimate their olfactory performance (in spite of olfactory impairment).…”

“…We also did not find any significant correlations between thresholds and clinical measures of disease severity or progression: UPDRS ('on' or 'off' medication), levodopa equivalent daily dose (LEDD; Tomlinson et al, 2010), or disease duration (p > 0.05 for all, before correction for multiple comparisons). These results suggest that PD deficits in complex visual motion paradigms, including biological motion (Jaywant et al, 2016) and 3D visual self-motion perception (Yakubovich et al, 2020) likely reflect more complex impairments of higher-level brain functions for interpreting visual motion, and not a basic visual motion perception deficit in PD.…”

“…Strikingly, despite broad visual impairments, PD patients seem to demonstrate increased reliance on visual cues (Cooke et al, 1978;Azulay et al, 2002;Vaugoyeau et al, 2007;Davidsdottir et al, 2008;Barnett-Cowan et al, 2010;Funato et al, 2010). In our laboratory, we recently found that PD patients over-weighted visual self-motion cues (even though these were impaired) when integrating them with vestibular cues (Yakubovich et al, 2020). Thus, PD may be marked by a central brain impairment in integrating sensory information (Bertolini et al, 2015;Halperin et al, 2020;Yakubovich et al, 2020).…”

“…In our laboratory, we recently found that PD patients over-weighted visual self-motion cues (even though these were impaired) when integrating them with vestibular cues (Yakubovich et al, 2020). Thus, PD may be marked by a central brain impairment in integrating sensory information (Bertolini et al, 2015;Halperin et al, 2020;Yakubovich et al, 2020).…”

“…These include: delays in visual evoked responses (Bodis-Wollner and Yahr, 1978), contrast abnormalities (Bodis-Wollner et al, 1987), deterioration of spatiotemporal and color sensitivity (Montse et al, 2001;Weil et al, 2016). In addition, altered perception of visual orientation and impaired visual perception of self-motion could impact mobility, gait and balance (Davidsdottir et al, 2008;Gullett et al, 2013;Lin et al, 2014;Halperin et al, 2020;Yakubovich et al, 2020). Strikingly, despite broad visual impairments, PD patients seem to demonstrate increased reliance on visual cues (Cooke et al, 1978;Azulay et al, 2002;Vaugoyeau et al, 2007;Davidsdottir et al, 2008;Barnett-Cowan et al, 2010;Funato et al, 2010).…”