Parkinson's disease alters multisensory perception: Insights from the Rubber Hand Illusion

Catherine Ding; Colin J Palmer; Jakob Hohwy; George J Youssef; Bryan Paton; Naotsugu Tsuchiya; Julie C Stout; Dominic Thyagarajan

doi:10.1016/j.neuropsychologia.2017.01.031

Parkinson's disease alters multisensory perception: Insights from the Rubber Hand Illusion

Neuropsychologia. 2017 Mar:97:38-45. doi: 10.1016/j.neuropsychologia.2017.01.031. Epub 2017 Jan 31.

Authors

Catherine Ding¹, Colin J Palmer², Jakob Hohwy², George J Youssef³, Bryan Paton⁴, Naotsugu Tsuchiya⁵, Julie C Stout⁵, Dominic Thyagarajan⁶

Affiliations

¹ Department of Neurosciences, School of Clinical Sciences, Monash Health, Clayton, Victoria 3168, Australia.
² Cognition & Philosophy Lab, Monash University, Clayton, Victoria 3800, Australia.
³ School of Psychology, Faculty of Health, Deakin University, Burwood, Victoria 3125, Australia.
⁴ Cognition & Philosophy Lab, Monash University, Clayton, Victoria 3800, Australia; Monash Institute of Cognitive and Clinical Neurosciences, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia.
⁵ Monash Institute of Cognitive and Clinical Neurosciences, School of Psychological Sciences, Monash University, Clayton, Victoria 3800, Australia.
⁶ Department of Neurosciences, School of Clinical Sciences, Monash Health, Clayton, Victoria 3168, Australia. Electronic address: dominic.thyagarajan@monash.edu.

PMID: 28153639
DOI: 10.1016/j.neuropsychologia.2017.01.031

Abstract

Background: Manipulation of multisensory integration induces illusory perceptions of body ownership. Patients with Parkinson's disease (PD), a neurodegenerative disorder characterised by striatal dopamine deficiency, are prone to illusions and hallucinations and have sensory deficits. Dopaminergic treatment also aggravates hallucinations in PD. Whether multisensory integration in body ownership is altered by PD is unexplored.

Objective: To study the effect of dopamine neurotransmission on illusory perceptions of body ownership.

Methods: We studied the Rubber Hand Illusion (RHI) in 21 PD patients (on- and off-medication) and 21 controls. In this experimental paradigm, synchronous stroking of a rubber hand and the subject's hidden real hand results in the illusory experience of 'feeling' the rubber hand, and proprioceptive mislocalisation of the real hand towards the rubber hand ('proprioceptive drift'). Asynchronous stroking typically attenuates the RHI.

Results: The effect of PD on illusory experience depended on the stroking condition (b = -2.15, 95% CI [-3.06, -1.25], p < .0001): patients scored questionnaire items eliciting the RHI experience higher than controls in the illusion-attenuating (asynchronous) condition, but not in the illusion-promoting (synchronous) condition. PD, independent of stroking condition, predicted greater proprioceptive drift (b = 15.05, 95% CI [6.05, 24.05], p = .0022); the longer the disease duration, the greater the proprioceptive drift. However, the RHI did not affect subsequent reaching actions. On-medication patients scored both illusion (critical) and mock (control) questionnaire items higher than when off-medication, an effect that increased with disease severity (log (OR) =.014, 95% CI [.01, .02], p < .0001).

Conclusion: PD affects illusory perceptions of body ownership in situations that do not typically induce them, implicating dopamine deficit and consequent alterations in cortico-basal ganglia-thalamic circuitry in multisensory integration. Dopaminergic treatment appears to increase suggestibility generally rather than having a specific effect on own-body illusions, a novel finding with clinical and research implications.

Keywords: Body ownership; Multisensory perception; Parkinson's disease; Rubber Hand Illusion.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Aged
Female
Humans
Illusions / physiology*
Male
Middle Aged
Parkinson Disease / complications*
Perceptual Disorders / etiology*
Proprioception / physiology*
Touch Perception / physiology*