Task specific inter-hemispheric coupling in human subthalamic nuclei

Abstract

Cortical networks and quantitative measures of connectivity are integral to the study of brain function. Despite lack of direct connections between left and right subthalamic nuclei (STN), there are apparent physiological connections. During clinical examination of patients with Parkinson’s disease (PD), this connectivity is exploited to enhance signs of PD, yet our understanding of this connectivity is limited. We hypothesized that movement leads to synchronization of neural oscillations in bilateral STN, and we implemented phase coherence, a measure of phase-locking between cortical sites in a narrow frequency band, to demonstrate this synchronization. We analyzed task specific phase synchronization and causality between left and right STN local field potentials (LFPs) recorded from both hemispheres simultaneously during a cued movement task in four subjects with PD who underwent Deep Brain Stimulation (DBS) surgery. We used a data driven approach to determine inter-hemispheric channel pairs and frequencies with a task specific increase in phase locking.We found significant phase locking between hemispheres in alpha frequency (8–12 Hz) in all subjects concurrent with movement of either hand. In all subjects, phase synchronization increased over baseline upon or prior to hand movement onset and lasted until the motion ceased. Left and right hand movement showed similar patterns. Granger causality (GC) at the phase-locking frequencies between synchronized electrodes revealed a unidirectional causality from right to left STN regardless of which side was moved.Phase synchronization across hemispheres between basal ganglia supports existence of a bilateral network having lateralized regions of specialization for motor processing. Our results suggest this bilateral network is activated by a unilateral motor program. Understanding phase synchronization in natural brain functions is critical to development of future DBS systems that augment goal directed behavioral function.

Striatal Dopaminergic Innervation Regulates Subthalamic Beta-Oscillations and Cortical-Subcortical Coupling during Movements: Preliminary Evidence in Subjects with Parkinson’s Disease

“…Of relevance, such subcortical cross hemispheric coherence was not modulated by movements, despite the differences in beta-power between STN+ and STN− (Figure 1A), and it did not mirror the movement-related drop of the cortical-subcortical coherence (Figure 2). Our findings are consistent with recent studies, though with different tasks, showing a lack of modulation of subcortical cross-hemispheric coupling in the beta-band during movements in subjects with PD (Darvas and Hebb, 2014; Kato et al, 2016). We speculate that such a persistent subcortical coherence might not be related to motor processing but relies upon a (bilateral) dopaminergic loss.…”

Metabolic, synaptic and behavioral impact of 5‐week chronic deep brain stimulation in hemiparkinsonian rats

“…; Walker et al . ; Darvas and Hebb ) and might be due, at least in part, to enhanced motivation for food and/or increased perseverative behavior, which is a known outcome of STN HFS (Baunez et al . ; Baunez and Gubellini ).…”

Frequency-Specific Synchronization in the Bilateral Subthalamic Nuclei Depending on Voluntary Muscle Contraction and Relaxation in Patients with Parkinson’s Disease

“…These frequency-specific movement-related ERD and ERS occur in the two STNs across hemispheres (Alegre et al, 2005 ), suggesting that bilateral STNs are involved with the initiation of a unilateral motor program. In addition, the alpha functional coupling between bilateral STNs increases prior to the onset of unilateral movement (Darvas and Hebb, 2014 ). This finding suggests that frequency-specific bilateral networks between the two STNs are activated for a unilateral motor program of VMC.…”