Irregularity of instantaneous gamma frequency in the motor control network characterize visuomotor and proprioceptive information processing

• Published in: Journal of neural engineering 2024-04, Vol.21 (2), p.26007
• Main Authors: Ryu, Jihye, Choi, Jeong Woo, Niketeghad, Soroush, Torres, Elizabeth B, Pouratian, Nader
• Format: Article
• Language: English
• Subjects: Electrocorticography; electrocorticography (ECoG); entropy; Fingers - physiology; goal-directed movement; Humans; instantaneous gamma frequency; motor network; Movement - physiology; Parietal Lobe; Proprioception - physiology; reaching
• ISSN: 1741-2560; 1741-2552; 1741-2552
• DOI: 10.1088/1741-2552/ad2e1d

The study aims to characterize movements with different sensory goals, by contrasting the neural activity involved in processing proprioceptive and visuo-motor information. To accomplish this, we have developed a new methodology that utilizes the irregularity of the instantaneous gamma frequency parameter for characterization. In this study, eight essential tremor patients undergoing an awake deep brain stimulation implantation surgery repetitively touched the clinician's finger (forward visually-guided/FV movement) and then one's own chin (backward proprioceptively-guided/BP movement). Neural electrocorticographic recordings from the motor (M1), somatosensory (S1), and posterior parietal cortex (PPC) were obtained and band-pass filtered in the gamma range (30-80 Hz). The irregularity of the inter-event intervals (IEI; inverse of instantaneous gamma frequency) were examined as: (1) auto-information of the IEI time series and (2) correlation between the amplitude and its proceeding IEI. We further explored the network connectivity after segmenting the FV and BP movements by periods of accelerating and decelerating forces, and applying the IEI parameter to transfer entropy methods. Conceptualizing that the irregularity in IEI reflects active new information processing, we found the highest irregularity in M1 during BP movement, highest in PPC during FV movement, and the lowest during rest at all sites. Also, connectivity was the strongest from S1 to M1 and from S1 to PPC during FV movement with accelerating force and weakest during rest. . We introduce a novel methodology that utilize the instantaneous gamma frequency (i.e. IEI) parameter in characterizing goal-oriented movements with different sensory goals, and demonstrate its use to inform the directional connectivity within the motor cortical network. This method successfully characterizes different movement types, while providing interpretations to the sensory-motor integration processes.