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

AbstractBackgroundParkinson’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.ObjectivesTo test self-motion perception in PD, separately for visual and vestibular cues (unisensory), and multisensory integration thereof.MethodsParticipants (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).ResultsPD 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 over-weighted visual cues during multisensory (visual-vestibular) integration.ConclusionsSelf-motion perception is affected already in early stage PD, specifically by impaired visual (vs. vestibular) function, and by suboptimal visual-vestibular integration. This may contribute to impaired balance and gait control. Future investigation into this connection might open up new avenues for alternative therapies to better treat these symptoms. Furthermore, these results may also impact early PD diagnosis and subtyping.

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

Brain Communications ◽

10.1093/braincomms/fcaa035 ◽

2020 ◽

Vol 2 (1) ◽

Cited By ~ 2

Author(s):

Sol Yakubovich ◽

Simon Israeli-Korn ◽

Orly Halperin ◽

Gilad Yahalom ◽

Sharon Hassin-Baer ◽

...

Keyword(s):

Parkinson’S Disease ◽

Parkinson's Disease ◽

Motion Perception ◽

Multisensory Integration ◽

Visual Cues ◽

Early Stage ◽

Disease Diagnosis ◽

Motion Platform ◽

Self Motion ◽

Better Than

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.

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Overconfidence in visual perception in Parkinson’s disease

10.1101/2020.09.09.289082 ◽

2020 ◽

Author(s):

Orly Halperin ◽

Roie Karni ◽

Simon Israeli-Korn ◽

Sharon Hassin-Baer ◽

Adam Zaidel

Keyword(s):

Parkinson’S Disease ◽

Parkinson's Disease ◽

Young Adult ◽

Motion Perception ◽

Multisensory Integration ◽

Visual Cues ◽

Visual Motion ◽

Visual Motion Perception ◽

The Right ◽

Future Work

AbstractBackgroundIncreased dependence on visual cues in Parkinson’s disease (PD) can unbalance the perception-action loop, impair multisensory integration, and affect everyday function of PD patients. It is currently unknown why PD patients seem to be more reliant on their visual cues.ObjectivesWe hypothesized that PD patients may be overconfident in the reliability (precision) of their visual cues. In this study we tested coherent visual motion perception in PD, and probed subjective (self-reported) confidence in their visual motion perception.Methods20 patients with idiopathic PD, 21 healthy aged-matched controls and 20 healthy young adult participants were presented with visual stimuli of moving dots (random dot kinematograms). They were asked to report: (1) whether the aggregate motion of dots was to the left or to the right, and (2) how confident they were that their perceptual discrimination was correct.ResultsVisual motion discrimination thresholds were similar (unimpaired) in PD compared to the other groups. By contrast, PD patients were significantly overconfident in their visual perceptual decisions (p=0.002 and p<0.001 vs. the age-matched and young adult groups, respectively).ConclusionsThese results suggest intact visual motion perception, but overestimation of visual cue reliability, in PD. Overconfidence in visual (vs. other, e.g., somatosensory) cues could underlie accounts of increased visual dependence and impaired multisensory integration in PD, and could contribute to gait and balance impairments. Future work should investigate PD confidence in somatosensory function. A better understanding of altered sensory reliance in PD might open up new avenues to treat debilitating symptoms.

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Examining the Effect of Age on Visual–Vestibular Self-Motion Perception Using a Driving Paradigm

Perception ◽

10.1177/0301006616675883 ◽

2016 ◽

Vol 46 (5) ◽

pp. 566-585 ◽

Cited By ~ 9

Author(s):

Robert Ramkhalawansingh ◽

Behrang Keshavarz ◽

Bruce Haycock ◽

Saba Shahab ◽

Jennifer L. Campos

Keyword(s):

Older Adults ◽

Motion Perception ◽

Multisensory Integration ◽

Visual Cues ◽

Lateral Position ◽

Control Group ◽

Younger Adults ◽

Age Related ◽

Vestibular Cues ◽

Self Motion

Previous psychophysical research has examined how younger adults and non-human primates integrate visual and vestibular cues to perceive self-motion. However, there is much to be learned about how multisensory self-motion perception changes with age, and how these changes affect performance on everyday tasks involving self-motion. Evidence suggests that older adults display heightened multisensory integration compared with younger adults; however, few previous studies have examined this for visual–vestibular integration. To explore age differences in the way that visual and vestibular cues contribute to self-motion perception, we had younger and older participants complete a basic driving task containing visual and vestibular cues. We compared their performance against a previously established control group that experienced visual cues alone. Performance measures included speed, speed variability, and lateral position. Vestibular inputs resulted in more precise speed control among older adults, but not younger adults, when traversing curves. Older adults demonstrated more variability in lateral position when vestibular inputs were available versus when they were absent. These observations align with previous evidence of age-related differences in multisensory integration and demonstrate that they may extend to visual–vestibular integration. These findings may have implications for vehicle and simulator design when considering older users.

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