Motor Synchronization to Rhythmic Auditory Stimulation (RAS) Attenuates Dopaminergic Responses in Ventral Striatum in Young Healthy Adults: [11C]-(+)-PHNO PET Study.

Yuko Koshimori,Vivek Sharma,Michael H Thaut,Sang-Soo Cho,Mikaeel Valli,Antonio P Strafella,Sylvain Houle

doi:10.3389/fnins.2019.00106

Abstract

Auditory-motor entrainment using rhythmic auditory stimulation (RAS) has been shown to improve motor control in healthy persons and persons with neurologic motor disorders such as Parkinson’s disease and stroke. Neuroimaging studies have shown the modulation of corticostriatal activity in response to RAS. However, the underlying neurochemical mechanisms for auditory-motor entrainment are unknown. The current study aimed to investigate RAS-induced dopamine (DA) responses in basal ganglia (BG) during finger tapping tasks combined with [11C]-(+)-PHNO-PET in eight right-handed young healthy participants. Each participant underwent two PET scans with and without RAS. Binding potential relative to the non-displaceable compartment (BPND) values were derived using the simplified reference tissue method. The task performance was measured using absolute tapping period error and its standard deviation. We found that the presence of RAS significantly improved the task performance compared to the absence of RAS, demonstrated by reductions in the absolute tapping period error (p = 0.007) and its variability (p = 0.006). We also found that (1) the presence of RAS reduced the BG BPND variability (p = 0.013) and (2) the absence of RAS resulted in a greater DA response in the left ventral striatum (VS) compared to the presence of RAS (p = 0.003), These suggest that the absence of external cueing may require more DA response in the left VS associated with more motivational and sustained attentional efforts to perform the task. Additionally, we demonstrated significant age effects on D2/3 R availability in BG: increasing age was associated with reduced D2/3 R availability in the left putamen without RAS (p = 0.026) as well as in the right VS with RAS (p = 0.02). This is the first study to demonstrate the relationships among RAS, DA response/D2/3 R availability, motor responses and age, providing the groundwork for future studies to explore mechanisms for auditory-motor entrainment in healthy elderly and patients with dopamine-based movement disorders.

Highlights

Rhythmic auditory stimulation (RAS) – presented either as single auditory beats or metronome clicks embedded in instrumental music – has shown to improve motor control in healthy persons and persons with neurologic motor disorders such as Parkinson’s disease (PD) and stroke (Miller et al, 1996; Thaut et al, 1996, 2002; McIntosh et al, 1997; Massie et al, 2009)
Our major findings include that the presentation of RAS significantly improved finger tapping task performance and that the presentation of RAS led to significantly reduced DA responses in the left ventral striatum (VS)
Consistent with our hypothesis, Binding potential relative to the non-displaceable compartment (BPND) values would significantly different between conditions in basal ganglia (BG)

Summary

Introduction

Rhythmic auditory stimulation (RAS) – presented either as single auditory beats or metronome clicks embedded in instrumental music – has shown to improve motor control in healthy persons and persons with neurologic motor disorders such as Parkinson’s disease (PD) and stroke (Miller et al, 1996; Thaut et al, 1996, 2002; McIntosh et al, 1997; Massie et al, 2009). Reduction in variability of motor timing, electromyography recruitment, and movement kinematics as well as increases in speed are among the positive effects demonstrated. These benefits result from rhythmic auditory entrainment. Entrainment refers to the frequency locking of two oscillating bodies that can move in stable periodic cycles (Thaut, 2015). The rhythmic frequency provides the brain (already equipped with internal time keeper mechanism) with an additional externally triggered time keeper, which generates a precise temporal interval as a continuous time reference (Thaut, 2015). The auditory system is more precise and faster to detect temporal patterns than other sensory systems such as visual and tactile systems (Shelton and Kumar, 2010)

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