Heightened orofacial, manual, and gait variability in Parkinson’s disease results from a general rhythmic impairment

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.

Evaluating a Speech-Specific and a Computerized Step-Training-Specific Rhythmic Intervention in Parkinson's Disease: A Cross-Over, Multi-Arms Parallel Study

“…Apart from strong correlations between parameters in speech and gait, this study also showed that rhythmic interventions, whatever their primary therapy focus, can bring about improvement in both dysfluent domains simultaneously. These findings are novel and may support the hypothesis of a common underlying rhythmic deficit (42,48,51,58). They are also in line with the consistent existing evidence (5, 9, 52, 53, 58-66, 91, 94, 95, 121) that rhythmic cues facilitate the retrieval and re-initiation of motor patterns in speech and gait having been impaired by the progression of PD.…”

“…Early research suggested that dysrhythmic speech in PD develops in line with spatiotemporal gait disorders, as motor articulation and speech rate decreases similarly to walking velocity (43)(44)(45)(46), and the inter-pause speech duration (ISD) shortens similarly to stride or step length (43,47,48), and also that paradoxical speech rhythms may be linked to gait festination and freezing (43,(48)(49)(50). Therefore, a common underlying dysrhythmic deficit in gait and speech in PD has been assumed and the term "general dysrhythmia" has been introduced (20,40,48,(50)(51)(52)(53).…”

Speech Rhythm Variation in Early-Stage Parkinson's Disease: A Study on Different Speaking Tasks

“…Furthermore, one of the most common symptoms is the alteration of speech rhythm and rate and speech/pause ratio, as part of a more "general dysrhythmia, " which has been often reported in patients with PD tested also in nonverbal rhythmic tasks, such as finger tapping and gait (Dalla Bella et al, 2018;De Cock et al, 2018;Puyjarinet et al, 2018Puyjarinet et al, , 2019.…”

About time: Ageing influences neural markers of temporal predictability

“…The general importance of sensory and sensorimotor timing abilities becomes evident when underlying mechanisms are affected by neural or psychological conditions, such as Parkinson's Disease (Benoit et al, 2014;Cunnington, Iansek, Bradshaw, & Phillips, 1995), schizophrenia (Carroll, Boggs, O'Donnell, Shekhar, & Hetrick, 2008), attention-deficit hyperactivity disorder (Dankner, Shalev, Carrasco, & Yuval-Greenberg, 2017;Hart et al, 2014), cerebellar (Ivry & Keele, 1989;Kotz, Stockert, & Schwartze, 2014) or basal ganglia lesions (Schwartze, Keller, Patel, & Kotz, 2011). For example, timing abilities are compromised in Parkinson's disease patients (Allman & Meck, 2011;Benoit et al, 2014;Dalla Bella et al, 2017;Puyjarinet et al, 2019), leading to impaired temporal predictions (Breska & Ivry, 2018). However, there are also indications that timing abilities vary over the lifespan and change systematically with age (McAuley, Jones, Holub, Johnston, & Miller, 2006).…”