Rhythmic auditory cues shape neural network recruitment in Parkinson's disease during repetitive motor behavior

Abstract

It is well established clinically that rhythmic auditory cues can improve gait and other motor behaviors in Parkinson's disease (PD) and other disorders. However, the neural systems underlying this therapeutic effect are largely unknown. To investigate this question we scanned people with PD and age-matched healthy controls using functional magnetic resonance imaging (fMRI). All subjects performed a rhythmic motor behavior (right hand finger tapping) with and without simultaneous auditory rhythmic cues at two different speeds (1 and 4 Hz). We used spatial independent component analysis (ICA) and regression to identify task-related functional connectivity networks and assessed differences between groups in intra- and inter-network connectivity. Overall, the control group showed greater intra-network connectivity in perceptual and motor related networks during motor tapping both with and without rhythmic cues. The PD group showed greater inter-network connectivity between the auditory network and the executive control network, and between the executive control network and the motor/cerebellar network associated with the motor task performance. We interpret our results as indicating that the temporal rhythmic auditory information may assist compensatory mechanisms through network-level effects, reflected in increased interaction between auditory and executive networks that in turn modulate activity in cortico-cerebellar networks.

Keywords: basal ganglia; beat; entrainment; music therapy; synchronization.

Figure 1:

Static visual displays accompanying each of the four the task conditions. Each display was presented at the beginning of the block and remained on the screen throughout the block without change. These visual displays were intended to orient the participants to the task; individual taps were cued only via auditory stimulation, not concurrent visual stimulation. In the Rhythmic Auditory Stimulation conditions (RAS), auditory stimulation continued throughout the 16 s block, as indicated by the red vertical cues that extend across the length of the green line. In the no-RAS conditions auditory stimulation was present only for the first 2 s and subjects were required to continue tapping at the indicated speed throughout the block. In the Fast conditions, subjects tapped at a rate of 4Hz; Slow conditions at a rate of 1 Hz.

Figure 2:

Eight task-modulated components identified via Spatial Group ICA that were retained for subsequent network-level analyses. For each spatial map, the familywise error rate was controlled at the voxel level (p < 0.05).

Figure 3:

Functional Network Connectivity. Top Left: Across all participants (Patients and Controls). Top Right: Significant differences between PD and control group. PD showed stronger connectivity between the visual and auditory networks, auditory and executive control networks, and between the executive control and motor/cerebellar networks than controls. Bottom left: PD group only. Bottom Right: Control group only. In all plots, only statistically significant connections are shown (FDR-corrected p-values < 0.05). Only the lower triangular portion of the symmetric correlation matrix is shown. Color bars indicate Pearson correlation coefficient values.