Abstract
Individuals with Parkinson’s disease (PD) experience rhythm disorders in a number of motor tasks, such as (i) oral diadochokinesis, (ii) finger tapping, and (iii) gait. These common motor deficits may be signs of “general dysrhythmia”, a central disorder spanning across effectors and tasks, and potentially sharing the same neural substrate. However, to date, little is known about the relationship between rhythm impairments across domains and effectors. To test this hypothesis, we assessed whether rhythmic disturbances in three different domains (i.e., orofacial, manual, and gait) can be related in PD. Moreover, we investigated whether rhythmic motor performance across these domains can be predicted by rhythm perception, a measure of central rhythmic processing not confounded with motor output. Twenty-two PD patients (mean age: 69.5 ± 5.44) participated in the study. They underwent neurological and neuropsychological assessments, and they performed three rhythmic motor tasks. For oral diadochokinesia, participants had to repeatedly produce a trisyllable pseudoword. For gait, they walked along a computerized walkway. For the manual task, patients had to repeatedly produce finger taps. The first two rhythmic motor tasks were unpaced, and the manual tapping task was performed both without a pacing stimulus and musically paced. Rhythm perception was also tested. We observed that rhythmic variability of motor performances (inter-syllable, inter-tap, and inter-stride time error) was related between the three functions. Moreover, rhythmic performance was predicted by rhythm perception abilities, as demonstrated with a logistic regression model. Hence, rhythm impairments in different motor domains are found to be related in PD and may be underpinned by a common impaired central rhythm mechanism, revealed by a deficit in rhythm perception. These results may provide a novel perspective on how interpret the effects of rhythm-based interventions in PD, within and across motor domains.
Highlights
Among the symptoms of idiopathic Parkinson’s disease (PD), patients often experience a poor appraisal of rhythmic events.When patients are asked to move spontaneously or to the beat of an auditory stimulus, timing deficits are found consistently in tasks such as manual tapping.[1]
These rhythmic abilities are known to engage subcortico-cortical networks involving the basal ganglia and the cerebellum,[1,2,3] some of which are affected in the progression of the disease
Rhythmic disorders in PD are found in other motor abilities, such as orofacial rhythmic coordination, where patients have difficulties in keeping a steady—isochronous—oral rhythm,[4] or gait, typically showing altered stride timing.[5]
Summary
When patients are asked to move spontaneously or to the beat of an auditory stimulus (e.g., a metronome or music), timing deficits are found consistently in tasks such as manual tapping.[1] These rhythmic abilities are known to engage subcortico-cortical networks involving the basal ganglia and the cerebellum,[1,2,3] some of which are affected in the progression of the disease. Rhythmic disorders in PD are found in other motor abilities, such as orofacial rhythmic coordination (e.g., oral diadochokinesis tasks), where patients have difficulties in keeping a steady—isochronous—oral rhythm,[4] or gait, typically showing altered stride timing.[5] Rhythm disorders in PD manifest in perceptual tasks, in the absence of motor output, such as extracting the beat from a musical sequence.[6,7] Altogether, these findings point towards a general rhythm disorder, so-called “general dysrhythmia”, putatively linked to the malfunctioning of a neural circuitry devoted to rhythm processing, which might characterize PD and manifest across different effectors.[8]
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