Movement-related changes in pallidocortical synchrony differentiate action execution and observation in humans

Abstract

Suppression of local and network alpha (8)(9)(10)(11)(12) and beta oscillations in the human basal ganglia-thalamocortical (BGTC) circuit is a prominent feature of movement. Local alpha/beta power, cross-region beta phase coupling, and phase-amplitude coupling (PAC) have all been shown to be suppressed during movement in multiple nodes of the BGTC. However, the specificity of these various movement-related changes to actual movement execution remains poorly understood. To differentiate signals that are specifically related to movement execution, we compared changes in globus pallidus internus (GPi) and motor cortical local oscillatory activity and coupling (cross-region phase coupling and local PAC) during movement execution and movement observation in 12 patients with Parkinson disease undergoing deep brain stimulator implantation. We hypothesized that network coupling is more directly related to movement execution than local power changes, given the putative role of pathological network coupling in movement disorders such as Parkinson disease. We observed suppression of alpha/beta power during action observation and execution in the globus pallidus and motor cortex during both action execution and action observation. In contrast, pallidocortical coherence and GPi and motor cortical alpha/beta-gamma PAC were significantly suppressed only during action execution. Our results demonstrate a functional dissociation within the BG-cortical network during action execution and observation in which suppression of BG-cortical functional connectivity and local phase amplitude coupling are features specifically of overt movement, suggesting a particularly important role in motor execution. This has implications for identification and use of intracranial signals for closed loop brain stimulation therapies.

GABAergic Modulation in Movement Related Oscillatory Activity: A Review of the Effect Pharmacologically and with Aging

“…MRGS is considered to be more associated with planning or initiation of movement than with its continuation [ 42 43 ]. Furthermore, excessive phase-amplitude-coupling (PAC) of alpha/beta frequencies with gamma frequencies in the motor cortex has been observed in hypokinetic disorders, such as Parkinson’s disease, and is believed to be one mechanism for the observed movement deficits in Parkinson’s disease [ 44 45 ]. Whereas, beta-ERS has been suggested to represent an inhibition of the motor cortex [ 46 ] or somatosensory reafference [ 47 ] for which there is debate as to the importance of GABAergic mediation [ 1 3 7 ].…”