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

Frédéric Puyjarinet; Valentin Bégel; Christian Gény; Valérie Driss; Marie-Charlotte Cuartero; Sonja A Kotz; Serge Pinto; Simone Dalla Bella

doi:10.1038/s41531-019-0092-6

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

NPJ Parkinsons Dis. 2019 Sep 25:5:19. doi: 10.1038/s41531-019-0092-6. eCollection 2019.

Authors

Frédéric Puyjarinet¹, Valentin Bégel², Christian Gény³, Valérie Driss⁴, Marie-Charlotte Cuartero⁵, Sonja A Kotz⁶, Serge Pinto^#⁵, Simone Dalla Bella^#^{1

7

8

9}

Affiliations

¹ 1EuroMov Laboratory, University of Montpellier, 700 Avenue du Pic Saint Loup, 34090 Montpellier, France.
² Charles-de-Gaulle University, Lille 3, 42 Rue Paul Duez, 59 000 Lille, France.
³ 3Neurology Department, CHRU of Montpellier, 80 Avenue Augustin Fliche, 34000 Montpellier, France.
⁴ 4Investigation Clinic Center, CHRU of Montpellier, 80 Avenue Augustin Fliche, 34000 Montpellier, France.
⁵ 5Aix Marseille Univ, CNRS, LPL, Aix-en-Provence, France.
⁶ 6Department of Neuropsychology and Psychopharmacology, University of Maastricht, Universiteitssingel, 6200 MD Maastricht, Netherlands.
⁷ 7International Laboratory for Brain, Music and Sound Research (BRAMS), 90 Vincent-d'Indy Ave., Outremont, QC H2V 2S9 Canada.
⁸ 8Department of Psychology, University of Montreal, 2900 Boulevard Edouard-Montpetit, Montréal, QCH3T 1J4 Montreal, Canada.
⁹ University of Economics and Human Sciences in Warsaw, Okopowa59, 01-043 Warsaw, Poland.

^# Contributed equally.

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.

Keywords: Neurological manifestations; Parkinson's disease.