Cognitive Factors Modulate Activity within the Human Subthalamic Nucleus during Voluntary Movement in Parkinson's Disease

Abstract

Movement is accompanied by changes in the degree to which neurons in corticobasal ganglia loops synchronize their activity within discrete frequency ranges. Although two principal frequency bands-beta (15-30 Hz) and gamma (60 -90 Hz)-have been implicated in motor control, the precise functional correlates of their activities remain unclear. Local field potential (LFP) recordings in humans with Parkinson's disease undergoing surgery for deep brain stimulation to the subthalamic nucleus (STN) indicate that spectral changes both anticipate movement and occur perimovement. The extent to which such changes are modulated by cognitive factors involved in making a correct response seems critical in characterizing the functional associations of these oscillations. Accordingly, by recording LFP activity from the STN in parkinsonian patients, we demonstrate that perimovement beta and gamma reactivity is modulated by task complexity in a dopamine-dependent manner, despite the dynamics of the movement remaining unchanged. In contrast, spectral changes occurring in anticipation of future movement were limited to the beta band and, although modulated by dopaminergic therapy, were not modulated by task complexity. Our findings suggest two dopamine-dependent processes indexed by spectral changes in the STN: (1) an anticipatory activity reflected in the beta band that signals the likelihood of future action but does not proactively change with the cognitive demands of the potential response, and (2) perimovement activity that involves reciprocal beta and gamma band changes and is not exclusively related to explicit motor processing. Rather perimovement activity can also vary with, and may reflect, the cognitive complexity of the task.

Subcortical roles in lexical task processing: Inferences from thalamic and subthalamic event‐related potentials

“…This appears in line also with previous derivations from DBS electrodes showing spectral activity changes on stimuli predictive for pending motor responses [Oswal et al, 2012[Oswal et al, , 2013Williams et al, 2003]. On a formal level, prime-stimuli open new task trials (regardless of their semantic content).…”

“…In this sense, they might be treated as "warning cues" allowing for the temporal segmentation of the task structure. This appears in line also with previous derivations from DBS electrodes showing spectral activity changes on stimuli predictive for pending motor responses [Oswal et al, 2012[Oswal et al, , 2013Williams et al, 2003]. Furthermore, this is reminiscent of previously suggested STN functions in behavioral switching, that is, preparing for controlled actions with a changing behavioral context and the suppression of automatic responses, allowing for targeted task control [Isoda and Hikosaka, 2008].…”

Single trial beta oscillations index time estimation

“…In addition, preliminary analyses also showed signatures of an effect in the gamma band, as in Bartolo et al (2014). As pointed out by an anonymous reviewer (see also Oswal et al, (2013), these effects could be due to participants holding the button depressed for a longer period of time in the trials categorized as long. As gamma and beta power seem to index independent components (Muthukumaraswamy, 2014), it is unlikely that differences in the way the key was pressed are driving the result.…”

Interaction of synchronized dynamics in cortex and basal ganglia in Parkinson's disease

“…However, frontal areas are also involved in the interaction between motor circuits of cortex and BG in the form of frontal interhemispheric coherence. These observations complement earlier observations of the frontal circuits’ impact on motor parts of BG (e.g., Oswal et al ., ).…”