Motor Timing Deficits in Sequential Movements in Parkinson Disease Are Related to Action Planning: A Motor Imagery Study

Abbruzzese G (2013) Motor Timing Deficits in Sequential Movements in Parkinson Disease Are Related to Action Planning: A Motor Imagery Study. PLoS ONE 8(9): e75454. doi:10.1371/journal.pone.0075454 Motor Timing Deficits in Sequential Movements in Parkinson Disease Are Related to Action Planning: A Motor Imagery Study Laura Avanzino 0 Elisa Pelosin 0 Davide Martino 0 Giovanni Abbruzzese 0 Natasha M. Maurits, University Medical Center Groningen UMCG, Netherlands 0 1 Department of Experimental Medicine, Section of Human Physiology and Centro Polifunzionale di Scienze Motorie, University of Genoa , Genoa , Italy , 2 Department of Neuroscience, Rehabilitation , Ophthalmology, Genetics, Maternal and Child Health , University of Genoa , Genoa , Italy , 3 Queen Elizabeth Hospital, South London NHS Trust , London , United Kingdom , 4 King's College Hospital , London , United Kingdom , 5 Centre for Neuroscience and Trauma, Queen Mary University of London , London , United Kingdom 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. - The subjective representation of the passage of time is critical for a variety of motor activities. When planning a complex motor action, the central nervous system should execute an accurate integration of temporal as well as spatial information. The neural network supporting motor timing comprises the lateral cerebellum, basal ganglia, and sensorimotor cortical areas [1-4]. Particularly, the basal ganglia and their associated subcortical dopaminergic system play a crucial role acting as a hypothetical internal clock that beats the rhythm when the movement is internally generated [5,6]. The role of the basal ganglia in timing is particularly relevant to individuals with idiopathic Parkinsons disease (PD), who exhibit temporal processing deficits [5,7] that may contribute to the breakdown in the spatiotemporal patterning of movements. Bradykinesia (slowness of movement initiation and execution), a cardinal symptom of PD, is particularly evident for internally generated sequential movements, and can benefit from the introduction of external rhythmic cues [8-10]. 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. Motor imagery corresponds to the mental rehearsal of a movement without overtly performing the respective action [11-13], and is thought to involve mainly processes of movement preparation, with reduced involvement of end-stage movement executionrelated processes [14,15]. Abnormal performance on motor imagery tasks has been demonstrated in patients with PD using different approaches, including behavioural, electrophysiological (transcranial magnetic stimulation and movement-related potentials) and functional imaging studies [16-19]. These studies have also highlighted changes in functional activation of circuits interconnecting frontal cortical areas and basal ganglia in relation to motor imagery tasks in PD patients, further supporting general abnormalities of motor planning in this condition [16,18,20-22]. Despite this body of evidence, the contribution of motor planning abnormalities to the performance of internally generated sequential movements has never been directly explored through the analysis of the temporal features of movement in PD. To shed more light on this aspect, we adopted a modified version of an established test for motor timing, i.e. the synchronization-continuation paradigm, by introducing a motor imagery task. The synchronizationcontinuation paradigm involves: i) a synchronization phase, in which subjects are asked to tap in synchrony with a train of tones separated by a constant inter-stimulus interval (ISI), and ii) a continuation phase, in which subjects are requested to continue tapping at the previous rate in the absence of the auditory cue. The addition of a motor imagery task to the classical synchronization-continuation paradigm aims at disentangling, within the entire process of sequential finger movement production (the classical continuation task), the phase of motor planning from that of movement execution. In the present study, during the continuation phase patients with PD and healthy volunteers were asked, on the basis of the information received and stored during the synchronization phase, to either materially perform the movement (execution task) or imagine performing it (imagery task). Further, since performance on the synchronization-continuation test is largely dependent on the duration of the inter-stimulus interval (ISI), we tested both a sub-second (metronome rate: 1.5 Hz, ISI: 666 ms) and a supra-second (metronome rate: 0.5 Hz, ISI: 2000 ms) inter-stimulus interval between the cues. Materials and Methods Ethical Statement All participants gave their written informed consent prior to their inclusion in this study. The experimental protocol was approved by the ethics committee of the University of Genoa (Protocol nr. 31/12) and was carried out in agreement with legal requirements and international norms (Declaration of Helsinki, 1964). Subjects Fourtee (...truncated)