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Timing of Activity in the Basal Ganglia Is More Important to Movement than Firing Rates

Key findings

  • During deep brain stimulation surgery, 12 patients with Parkinson's disease performed a handgrip task as researchers recorded electrocorticographic and subthalamic nucleus unit activity
  • Elevated subthalamic nucleus spike-to-cortical gamma phase coupling preceded faster reaction times
  • This effect was most pronounced over the motor cortex, higher for fast movement than for slow movement and more pronounced for contralateral interactions than for ipsilateral interactions
  • There were no correlations between reaction times and firing rates in the same time window, indicating that the timing of neuronal discharges with respect to cortical gamma phase was more predictive of movement than firing rates were

How different regions of the brain work together to coordinate movement still isn't well understood. Such information is essential to efforts to improve treatments for Parkinson's disease and other basal ganglia disorders.

Several studies have documented strong correlations between movement kinematics and gamma-band activity in the basal ganglia. However, most research into single neuron activity during movement preparation and execution in the basal ganglia has focused on changes in firing rates, in line with current models of basal ganglia function. Less is known about how single neurons in the basal ganglia interact with functionally related brain areas through oscillatory coherence.

Mark Richardson, MD, PhD, the director of Functional Neurosurgery at Massachusetts General Hospital, in collaboration with Petra Fischer, PhD, of the John Radcliffe Hospital at University of Oxford, and colleagues set out to understand the mechanism of cortico–subcortical communication that may be linked to gamma-band activity. By studying patients undergoing neurosurgery for Parkinson's disease, they were able to examine interactions between the motor cortex and subthalamic nucleus (STN) neuron activity during a motor task. In eLife, the researchers report increased interaction between subcortex and cortex as a function of movement and movement speed.

Methods

Twelve patients with Parkinson's disease participated in a visually cued task in which they squeezed a handgrip with their left or right hand during deep brain stimulation surgery. Meanwhile, the researchers made concurrent electrocorticographic and STN unit recordings. They then analyzed electrophysiologic patterns associated with the movements and correlated these patterns with measures of behavioral performance.

Results

Elevated STN spike-to-cortical gamma phase coupling, already evident at the "go" cue for hand gripping, preceded faster reaction times. This observation suggests a role for subcortico–cortical coupling in preparing movement.

The STN spike-to-cortical gamma phase coupling was:

  • Most pronounced over the motor cortex
  • Higher for fast movement than for slow movement
  • More pronounced for contralateral interactions than for ipsilateral interactions

There were no correlations between reaction times and firing rates in the same time window, indicating that the timing of neuronal discharges with respect to cortical gamma phase was more predictive of movement than firing rates were.

Future Directions

These findings support the emerging concept that specific patterns of oscillatory synchronization can entrain neuronal spikes at different stages of motor control to facilitate or restrict motor output. Gamma oscillations may reflect the processing necessary for a change in motor state, such as the start of a movement or sudden cessation.

Ongoing research, supported by the Brain Research through Advancing Innovative Neurotechnologies (BRAIN) Initiative, applies multi-neuron recording and analysis techniques to explore the role of basal ganglia-cortical interactions in the uniquely human behavior of speech.

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