Interaction of motor behaviour, cortical oscillations and deep brain stimulation in Parkinson disease

Abstract

Abstract Recent progress in the study of Parkinson's disease (PD) has highlighted the pivotal role of beta oscillations within the basal ganglia-thalamo-cortical network in modulating motor symptoms. Predominantly manifesting as transient bursts, these beta oscillations are central to the pathophysiology of PD motor symptoms, especially bradykinesia. Our central hypothesis is that increased bursting duration in cortex, coupled with kinematics of movement, disrupts the typical flow of neural information, leading to observable changes in motor behavior in PD. To explore this hypothesis, we employed an integrative approach, analyzing the interplay between moment-to-moment brain dynamics and movement kinematics, and the modulation of these relationships by therapeutic deep brain stimulation (DBS). Local field potentials were recorded from the hand motor (M1) and premotor cortical (PM) areas, and internal Globus Pallidus (GPi) in 26 PD patients undergoing DBS implantation surgery. Participants executed rapid alternating hand movements in 30-second blocks, both with and without therapeutic pallidal stimulation. Behaviorally, the analysis revealed bradykinesia, with hand movement cycle width increasing linearly over time during DBS-OFF blocks. Crucially, there was a moment-to-moment correlation between M1 low beta burst duration and movement cycle width, a relationship that dissipated with therapeutic DBS. Further analyses suggest that high gamma activity correlates with enhanced motor performance with DBS-ON. Regardless of the nature of coupling, DBS’s modulation of cortical bursting activity appeared to amplify the brain signals’ informational content regarding instantaneous movement changes. Our findings underscore that DBS significantly reshapes the interaction between motor behavior and neural signals in PD, not only modulating specific bands but also expanding the system's capability to process and relay information for motor control. These insights shed light on the possible network mechanisms underlying DBS therapeutic effects, suggesting a profound impact on both neural and motor domains.