Abstract

People with Parkinson’s disease (PD) experience motor symptoms that are affected by sensory information in the environment. Sensory attenuation describes the modulation of sensory input caused by motor intent. This appears to be altered in PD and may index important sensorimotor processes underpinning PD symptoms. We review recent findings investigating sensory attenuation and reconcile seemingly disparate results with an emphasis on task-relevance in the modulation of sensory input. Sensory attenuation paradigms, across different sensory modalities, capture how two identical stimuli can elicit markedly different perceptual experiences depending on our predictions of the event, but also the context in which the event occurs. In particular, it appears as though contextual information may be used to suppress or facilitate a response to a stimulus on the basis of task-relevance. We support this viewpoint by considering the role of the basal ganglia in task-relevant sensory filtering and the use of contextual signals in complex environments to shape action and perception. This perspective highlights the dual effect of basal ganglia dysfunction in PD, whereby a reduced capacity to filter task-relevant signals harms the ability to integrate contextual cues, just when such cues are required to effectively navigate and interact with our environment. Finally, we suggest how this framework might be used to establish principles for effective rehabilitation in the treatment of PD.

Highlights

  • People with Parkinson’s Disease (PD) face debilitating symptoms that often begin years before disease diagnosis [1], worsen over time and significantly affect quality of life

  • The medium spiny neurons (MSNs) were more active for successful trials compared to unsuccessful, indicating that a motor response could be elicited with a predictive sensory stimuli [29]. It was the MSNs in the direct pathway—the pathway that is underactive in PD—that depolarised with the whiskers and predicted a licking response [125]

  • We have reviewed sensory attenuation through the lens of PD with a particular interest in sport and rehabilitation

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Summary

Introduction

People with Parkinson’s Disease (PD) face debilitating symptoms that often begin years before disease diagnosis [1], worsen over time and significantly affect quality of life. Dopamine replacement therapy is used to treat PD and can be effective for long periods [2], though it does not improve all cardinal symptoms of this neurodegenerative disorder [3], with high levels of wearing off over time and considerable dissatisfaction among patients [2] While techniques such as deep brain stimulation can be employed with relative success [4], they are still associated with significant shortfalls [5], not least of which are the narrow inclusion criteria deemed necessary for high efficacy [6], and the significant investment in time required for effective stimulator titration. We re-examine the literature with an explicit consideration of Task-Relevance and reframe sensory attenuation as the distinct context-dependent perception of two identical stimuli We propose that this novel framing reconciles a previously contradictory literature whilst still incorporating the concept of movement modulating sensory input. Implications for rehabilitation design are considered, pointing to sensory attenuation paradigms of a particular design to help monitor changes in important sensorimotor processing throughout an exercise programme

Recent and Relevant Findings
Reconsidering Sensory Attenuation Theory
Scope of the Dominant Theories
Factors Affecting Sensory Attenuation
Task-Relevance in Sensory Attenuation
Visualising
Neural Substrate
The BG through a Sensory Lens
Sensation to Action
Sensorimotor Integration
Establishing Principles for Rehabilitation
Conclusions
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