Motor timing deficits in sequential movements in Parkinson disease are related to action planning: a motor imagery study

Abstract

Timing of sequential movements is altered in Parkinson disease (PD). Whether timing deficits in internally generated sequential movements in PD depends also on difficulties in motor planning, rather than merely on a defective ability to materially perform the planned movement is still undefined. To unveil this issue, we adopted a modified version of an established test for motor timing, i.e. the synchronization-continuation paradigm, by introducing a motor imagery task. Motor imagery is thought to involve mainly processes of movement preparation, with reduced involvement of end-stage movement execution-related processes. Fourteen patients with PD and twelve matched healthy volunteers were asked to tap in synchrony with a metronome cue (SYNC) and then, when the tone stopped, to keep tapping, trying to maintain the same rhythm (CONT-EXE) or to imagine tapping at the same rhythm, rather than actually performing it (CONT-MI). We tested both a sub-second and a supra-second inter-stimulus interval between the cues. Performance was recorded using a sensor-engineered glove and analyzed measuring the temporal error and the interval reproduction accuracy index. PD patients were less accurate than healthy subjects in the supra-second time reproduction task when performing both continuation tasks (CONT-MI and CONT-EXE), whereas no difference was detected in the synchronization task and on all tasks involving a sub-second interval. Our findings suggest that PD patients exhibit a selective deficit in motor timing for sequential movements that are separated by a supra-second interval and that this deficit may be explained by a defect of motor planning. Further, we propose that difficulties in motor planning are of a sufficient degree of severity in PD to affect also the motor performance in the supra-second time reproduction task.

Figure 1. Experimental paradigm.

In our modified version of a synchronization-continuation task, subjects were requested to tap in synchrony with a metronome cue (SYNC) and then, when the tone stopped, to tap the fingers in a sequential order, trying to maintain the same rhythm as accurately as possible (CONT-EXE) or to imagine finger tapping at the same rhythm, rather than actually performing it (CONT-MI). The order of the tasks was random.

Figure 2. Temporal error expressed in ms.

Data of both patients with Parkinson’s disease (PD) and healthy control subjects (HS) are shown. The results of the synchronization (SYNC), execution (CONT-EXE) and motor imagery (CONT-MI) tasks with a supra-second (0.5 Hz) and sub-second (1.5 Hz) time interval are shown. On the x-axis, we show the type of task. On the y-axis, we show the duration of the temporal error. Asterisk indicates differences between PD and HS when interaction of TIME INTERVAL*GROUP* TASK was statistically significant (*p<0.05). Mean data + standard error mean (SEM) are shown.

Figure 3. Interval reproduction accuracy index (IRA).

Data of both patients with Parkinson’s disease (PD) and healthy control subjects (HS) are shown. The results of the synchronization (SYNC), execution (CONT-EXE) and motor imagery (CONT-MI) tasks with a supra-second (0.5 Hz) and sub-second (1.5 Hz) are shown. On the x-axis, we show the type of task. On the y-axis, we show the IRA expressed as a ratio between the time interval reproduced by the subject and the time interval set by the metronome. Asterisk indicates differences between PD and HS when interaction of TIME INTERVAL*GROUP* TASK was statistically significant (*p<0.05). Mean data + standard error mean (SEM) are shown.