Subthalamic nucleus deep brain stimulation in the beta frequency range boosts cortical beta oscillations and slows down movement

Recordings from Parkinson’s disease (PD) patients typically show strong beta-band oscillations (13-35Hz), which can be modulated by deep brain stimulation (DBS). While high-frequency DBS (>100Hz) ameliorates motor symptoms and reduces beta activity in basal ganglia and motor cortex, the effects of low-frequency DBS (<30Hz) are less clear. Clarifying these effects is relevant for the debate about the role of beta oscillations in motor slowing, which might be causal or epiphenomenal. Here, we investigated how subthalamic nucleus (STN) beta-band DBS affects cortical beta oscillations and motor performance. We recorded the magnetoencephalogram of 14 PD patients (9 males) with DBS implants while on their usual medication. Following a baseline recording (DBS off), we applied bipolar DBS at beta frequencies (10, 16, 20, 26, and 30Hz) via the left electrode in a cyclic fashion, turning stimulation on (5s) and off (3s) repeatedly. For each frequency, cyclic stimulation was applied at rest and during right hand finger tapping. In the baseline recording, we observed a negative correlation between the strength of hemispheric beta power lateralization and the tap rate. Importantly, beta-band DBS accentuated the lateralization and reduced the tap rate proportionally. The change in lateralization was specific to the alpha/beta range (8-26Hz), outlasted stimulation and did not depend on the stimulation frequency, suggesting a remote induced response rather than entrainment. Our study demonstrates that cortical beta oscillations can be manipulated by STN beta-band DBS. Importantly, this manipulation appears to have consequences for motor performance, supporting a causal role of beta oscillations in motor control. Significance Statement The slowing of movement in Parkinson’s disease is known to be related to pathologically enhanced neural oscillations in the beta range (13-35Hz). Whether these oscillations are the cause of motor slowing, however, remains debated. Here, we stimulated the brains of Parkinson patients in the beta range, using their implanted deep brain stimulator. Consistent with a causal effect, stimulation slowed down finger tapping. Additionally, the subcortical stimulation affected the hemispheric balance of beta oscillations in the remote motor cortices. The stronger the shift, the stronger was the slowing. These results suggest that subcortical beta-band stimulation causes motor slowing by boosting motor cortical beta oscillations, indicating that beta oscillations might indeed be “a bad boy in Parkinson’s disease”.