Temporal dynamics of motor integration in Parkinson's disease: towards a concept of time-frequency coding in cortico-basal networks

Introduction. Intraoperative recordings of oscillatory activity from the left subthalamic nucleus (STN), EEG and right forearm EMG (flexor digitorum muscle (FD), extensor digitorum muscle (ED)) were performed in six PD patients during surgery for STN-DBS in order to comprehensively study temporal dynamics of motor integration in distributed networks including STN, M1, and contralateral effector muscles.

Material and Methods: Randomised and externally paced finger movements of the right fingers 2–5 were performed. Temporal dynamics were quantified in terms of short time Fourier transform and event-related coherence analysis (using a sliding window technique) expressing local changes of activity (power) and neuronal synchronisation between distant oscillators (coherence). Data from the motor condition were referenced to the baseline condition at rest.

Results: Power analysis indicated a strong desynchronization of STN-activity 200–300ms before finger tap (10–40Hz). An increase in STN power (60–100Hz) was observed in single patients (n=2). Coherence between STN and contralateral forearm muscles showed differenzial patterns: STN-FD coherence was dominated by an increase of coherence in the beta band 300ms before finger tap, and inversely, STN-ED coherence desynchronized within the respective time range. Coherence between STN and the ipsilateral M1 desynchronized between 10–40Hz preceding the finger tap for up to 400ms and synchronized between 60 and 100Hz in the same time range. This reversed to baseline spectrum 100–200ms after the finger tap. Corticomuscular coherence between M1 and contralateral FD and ED increased in the beta band (10–20Hz) beginning 100ms before finger tap and persisted for approximately 200ms.

Conclusion: The present study demonstrates temporal dynamics of motor integration in functional neuronal and neuromuscular networks including STN, M1, and effector muscles. Modulation of neuronal activity and connectivity within a broad range of beta band activity was temporally linked to the motor program. Of note, the functional significance of synchrony in this frequency range varied upon projections (presumably antikinetic function in STN-M1 projections, prokinetic in STN-muscle projections and M1-muscle projections). Antagonistic muscular activity (FD vs. ED) within motor programs might be driven selectively and functionally by temporally dynamic frequency coding in STN-muscle projections.