Scaling of Movement Is Related to Pallidal γ Oscillations in Patients with Dystonia

Abstract

Neuronal synchronization in the gamma (␥) band is considered important for information processing through functional integration of neuronal assemblies across different brain areas. Movement-related ␥ synchronization occurs in the human basal ganglia where it is centered at ϳ70 Hz and more pronounced contralateral to the moved hand. However, its functional significance in motor performance is not yet well understood. Here, we assessed whether event-related ␥ synchronization (ERS) recorded from the globus pallidus internus in patients undergoing deep brain stimulation for medically intractable primary focal and segmental dystonia might code specific motor parameters. Pallidal local field potentials were recorded in 22 patients during performance of a choice-reaction-time task. Movement amplitude of the forearm pronation-supination movements was parametrically modulated with an angular degree of 30°, 60°, and 90°. Only patients with limbs not affected by dystonia were tested. A broad contralateral ␥ band (35-105 Hz) ERS occurred at movement onset with a maximum reached at peak velocity of the movement. The pallidal oscillatory ␥ activity correlated with movement parameters: the larger and faster the movement, the stronger was the synchronization in the ␥ band. In contrast, the event-related decrease in beta band activity was similar for all movements. Gamma band activity did not change with movement direction and did not occur during passive movements. The stepwise increase of ␥ activity with movement size and velocity suggests a role of neuronal synchronization in this frequency range in basal ganglia control of the scaling of ongoing movements.

Interhemispheric difference of pallidal local field potential activity in cervical dystonia

“…LFP power in the 11–30 Hz band has also been shown to correlate with dystonic EMG activity in patients with dystonia 11. Not only is this frequency band prominently involved in movement,17 but pallidal oscillatory 18–30 Hz activity recorded from DBS electrodes was desynchronised related to voluntary movements in patients with dystonia 18. Therefore, it is possible that the interhemispheric differences we found in this band may relate to the corrected and fixed head position of CD patients during DBS surgery.…”

Decoding gripping force based on local field potentials recorded from subthalamic nucleus in humans

“…Surgical subcortical targets, such as the STN and globus pallidus (GPi), are involved in motor planning and execution. Activities from STN and GPi have been shown to correlate with movement parameters such as movement amplitude and speed (Brücke et al, 2012; Joundi et al, 2012), and are also modulated by movement intention (Kühn et al, 2006). Basal ganglia output has been theorized to regulate movement gain in healthy motor control, and can contain important information about the motor vigour (Shadmehr and Krakauer, 2008; Turner and Desmurget, 2010).…”

“…Direct recordings from basal ganglia targets in patients suggest that changes in frequency specific activities in the local field potential (LFP) contribute to the selection of effort or force levels for voluntary movements. For example, the power over the gamma band (60–80 Hz) in the LFP in the globus pallidus correlates with the movement amplitude and velocity of the contralateral hand of patients with cranial dystonia (Brücke et al, 2012). Similar correlations have been noted in patients with Parkinson’s disease between movement speed and the power in the gamma band in the LFP picked up from the STN (Joundi et al, 2012).…”

Complementary roles of cortical oscillations in automatic and controlled processing during rapid serial tasks

“…It should be noted that, without EMG recordings, we cannot rule out the possibility of differences in movement parameters, such as force or speed, and sensorimotor gamma has been shown to be sensitive to these kinematic parameters such as movement amplitude in previous studies (Brucke et al, 2012;Joundi et al, 2012;Muthukumaraswamy, 2010). However, if gamma reflected differences in kinematic parameters, we would expect similar if not greater sensitivity to these differences in the motor field and movement-evoked fields, yet these measures were similar across tasks and trial types ( Supplementary Fig.…”