Spatial propagation of movement-related basal ganglia activity predicts parkinsonian motor state

Movement-related gamma activity (> 60 Hz) in cortico-basal ganglia networks reflects pro-kinetic synchronization dynamics. While in the cortex these temporal dynamics are known to unfold spatially across topographically distributed networks, it remains unclear whether a similar spatial propagation occurs within the basal ganglia, and how such spatial encoding may contribute to both physiological and disease-related mechanisms. The subthalamic nucleus (STN) is a key integrative hub for motor processing within the basal ganglia-cortical circuitry. At rest, STN activity is topographically distributed according to its spectral frequency components. To assess whether this spectral topography is dynamic and underlies movement encoding, we dissected the spatiotemporal properties of STN local field potentials recorded intraoperatively at rest and during movement across 63 hemispheres from patients with Parkinson’s disease. Using multi-contact deep brain stimulation leads, we captured high-resolution anatomical signal dynamics and contrasted a broad frequency spectrum (60–400 Hz), including high-gamma, fast-gamma, slow high-frequency oscillations and fast high-frequency oscillations. Moreover, we compared these signals to upper limb muscle activity and movement-related beta desynchronization, and examined their association with clinical impairment and levodopa responsiveness. All sub-bands exhibited significant movement-related synchronization in both the contralateral and ipsilateral STN, however, with distinct magnitude and temporal dynamics. The presence and degree of temporal locking to muscle activity and inverse relationship to movement-related beta desynchronization also varied by sub-band. Importantly, each sub-band exhibited spatially segregated hotspots located within the STN that propagate primarily along the inferior-superior axis, yet in band-specific directions. This spatial propagation evolved throughout the movement period but temporally decoupled from synchronization magnitude, indicating that spatial dynamics reflect a distinct property relevant for motor encoding. Notably, propagation of frequencies above 110 Hz inversely correlated with dopamine-related motor improvement, suggesting that exaggerated spatial dynamics may reflect compensatory mechanisms secondary to neurodegeneration. These findings demonstrated that synchronization within the basal ganglia is not a spatially static phenomenon but rather unfolds in space which expands on the current understanding of the basal ganglia mechanism. Propagation of movement-related activity may serve as a potential marker for motor impairment in Parkinson’s disease, opening new avenues for spectro-behavioural research and spatially informed neuromodulation strategies.