Differential components of bradykinesia in Parkinson's disease revealed by deep brain stimulation

Abstract

Bradykinesia is a term describing several manifestations of movement disruption caused by Parkinson's disease (PD), including movement slowing, amplitude reduction, and gradual decrease of speed and amplitude over multiple repetitions of the same movement. Deep brain stimulation (DBS) of the subthalamic nucleus (STN) improves bradykinesia in patients with PD. We examined the effect of DBS on specific components of bradykinesia when applied at two locations within the STN, using signal processing techniques to identify the time course of amplitude and frequency of repeated hand pronation-supination movements performed by participants with and without PD. Stimulation at either location increased movement amplitude, increased frequency, and decreased variability, though not to the range observed in the control group. Amplitude and frequency showed decrement within trials, which was similar in PD and control groups and did not change with DBS. Decrement across trials, by contrast, differed between PD and control groups, and was reduced by stimulation. We conclude that DBS improves specific aspects of movement that are disrupted by PD, whereas it does not affect short-term decrement that could reflect muscular fatigue.NEW & NOTEWORTHY In this study, we examined different components of bradykinesia in patients with Parkinson's disease (PD). We identified different components through signal processing techniques and their response to deep brain stimulation (DBS). We found that some components of bradykinesia respond to stimulation, whereas others do not. This knowledge advances our understanding of brain mechanisms that control movement speed and amplitude.

Keywords: DBS; kinematics; motor control; movement; wearable sensors.

Graphical abstract

Figure 1.

Sample kinematic data and signal processing for a single control (CTL) participant and a single Parkinson’s disease (PD) participant. A: time course of wrist angle (angular position in the pronation-supination range) in the DBS-Off condition for 3 hand rotation trials. Upper trace (gray) = CTL participant; lower trace (black) = PD patient. The x axis for all graphs in the figure is the horizontal axis at the bottom of the figure. Traces for the control participant and for the PD patient are offset from one another vertically offset for clarity; see calibration bars for scale. B: wrist angle in the dorsal DBS-On condition. C: wrist angle in the ventral DBS-On condition. D: amplitude, in the DBS-Off condition, of the analytic signal obtained by applying the Hilbert transform to the signal in A–C. E: Hilbert-transform amplitude in the dorsal DBS-On condition. F: Hilbert-transform amplitude in the ventral DBS-On condition. G: instantaneous frequency, in the DBS-Off condition, of the analytic signal obtained by applying the Hilbert transform to the signal in A–C. H: Hilbert-transform instantaneous frequency in the dorsal DBS-On condition. I: Hilbert-transform instantaneous frequency in the ventral DBS-On condition. DBS, deep brain stimulation.

Figure 2.

Power spectrum (frequency range 1–10 Hz) for the same pair of single participants as in Fig. 1 in the Off (A), Dorsal On (B), Ventral On (C) conditions. Gray trace = CTL participant; black trace = PD participant.

Figure 3.

Group mean of power spectrum for control (CTL) and for Parkinson’s disease (PD) groups in the Off, Dorsal On, Ventral On conditions. Shading indicates ±standard error. Solid red trace = CTL; solid black trace = PD, off condition; solid green trace = PD, dorsal-on condition; dashed blue trace = PD, ventral-on condition.

Figure 4.

Group mean of envelope amplitude for control (CTL) and for Parkinson’s disease (PD) groups in the Off, Dorsal On, Ventral On conditions. Shading indicates ±standard error. Solid red trace = CTL; solid black trace = PD, off condition; solid green trace = PD, dorsal-on condition; dashed blue trace = PD, ventral-on condition.

Figure 5.

Group mean of instantaneous frequency for control (CTL) and for Parkinson’s disease (PD) groups in the Off, Dorsal On, Ventral On conditions. Shading indicates ±standard error. Solid red trace = CTL; solid black trace = PD, off condition; solid green trace = PD, dorsal-on condition; dashed blue trace = PD, ventral-on condition.

Figure 6.

Signal processing quantities (means ± SD) for control (CTL) and Parkinson’s disease (PD) groups across trials and sessions. Circles = CTL group; triangles = PD group.