Primary Sensorimotor Cortex Drives the Common Cortical Network for Gamma Synchronization in Voluntary Hand Movements

Gertrúd Tamás, Venkata C. Chirumamilla, Abdul R. Anwar, Jan Raethjen, Günther Deuschl, Sergiu Groppa, Muthuraman Muthuraman

Background: Gamma synchronization (GS) may promote the processing between functionally related cortico-subcortical neural populations. Our aim was to identify the sources of GS and to analyze the direction of information flow in cerebral networks at the beginning of phasic movements, and during medium-strength isometric contraction of the hand. Methods: We measured 64-channel electroencephalography in 11 healthy volunteers (age: 25 ± 8 years; four females); surface electromyography detected the movements of the dominant hand. In Task 1, subjects kept a constant medium-strength contraction of the first dorsal interosseus muscle, and performed a superimposed repetitive voluntary self-paced brisk squeeze of an object. In Task 2, brisk, and in Task 3, constant contractions were performed. Time-frequency analysis of the EEG signal was performed with the multitaper method. GS sources were identified in five frequency bands (30-49, 51-75, 76-99, 101-125, and 126-149 Hz) with beamformer inverse solution dynamic imaging of coherent sources. The direction of information flow was estimated by renormalized partial directed coherence for each frequency band. The data-driven surrogate test, and the time reversal technique were performed to identify significant connections. Results: In all tasks, we depicted the first three common sources for the studied frequency bands that were as follows: contralateral primary sensorimotor cortex (S1M1), dorsolateral prefrontal cortex (dPFC) and supplementary motor cortex (SMA). GS was detected in narrower low- (∼30-60 Hz) and high-frequency bands (>51-60 Hz) in the contralateral thalamus and ipsilateral cerebellum in all three tasks. The contralateral posterior parietal cortex was activated only in Task 1. In every task, S1M1 had efferent information flow to the SMA and the dPFC while dPFC had no detected afferent connections to the network in the gamma range. Cortical-subcortical information flow captured by the GS was dynamically variable in the narrower frequency bands for the studied movements. Conclusion: A distinct cortical network was identified for GS in voluntary hand movement tasks. Our study revealed that S1M1 modulated the activity of interconnected cortical areas through GS, while subcortical structures modulated the motor network dynamically, and specifically for the studied movement program.