Cortico-pallidal oscillatory connectivity in patients with dystonia

Abstract

Primary dystonia has been associated with an underlying dysfunction of a wide network of brain regions including the motor cortex, basal ganglia, cerebellum, brainstem and spinal cord. Dystonia can be effectively treated by pallidal deep brain stimulation although the mechanism of this effect is not well understood. Here, we sought to characterize cortico-basal ganglia functional connectivity using a frequency-specific measure of connectivity-coherence. We recorded direct local field potentials from the human pallidum simultaneously with whole head magnetoencephalography to characterize functional connectivity in the cortico-pallidal oscillatory network in nine patients with idiopathic dystonia. Three-dimensional cortico-pallidal coherence images were compared to surrogate images of phase shuffled data across patients to reveal clusters of significant coherence (family-wise error P < 0.01, voxel extent 1000). Three frequency-specific, spatially-distinct cortico-pallidal networks have been identified: a pallido-temporal source of theta band (4-8 Hz) coherence, a pallido-cerebellar source of alpha band (7-13 Hz) coherence and a cortico-pallidal source of beta band (13-30 Hz) coherence over sensorimotor areas. Granger-based directionality analysis revealed directional coupling with the pallidal local field potentials leading in the theta and alpha band and the magnetoencephalographic cortical source leading in the beta band. The degree of pallido-cerebellar coupling showed an inverse correlation with dystonic symptom severity. Our data extend previous findings in patients with Parkinson's disease describing motor cortex-basal ganglia oscillatory connectivity in the beta band to patients with dystonia. Source coherence analysis revealed two additional frequency-specific networks involving the temporal cortex and the cerebellum. Pallido-cerebellar oscillatory connectivity and its association with dystonic symptoms provides further confirmation of cerebellar involvement in dystonia that has been recently reported using functional magnetic resonance imaging and fibre tracking.

Reply: Oscillatory coupling of the subthalamic nucleus in obsessive compulsive disorder

“…Hence, the reported coherence between the STN and sensorimotor cortex does not contradict the notion of beta oscillations being-at least predominantly-of motor significance within the cortex-basal ganglia loop. This is further supported by our recent studies in patients with dystonia where pallidocortical beta-band coherence is predominantly found to motor cortical areas (Neumann et al, 2015). This pallidocortical beta-band coherence is significantly reduced with movement, and the degree of beta-band coherence correlates with reaction times, which further supports a role in motor behaviour (van Wijk et al, 2017, in press).…”

“…Taken together, the evidence does not lead to the conclusion that beta oscillations per se are related to motor processing alone, but only that they have a distinctive significance within the motor system, as they are consistently found to mediate synchronization between cortical motor regions and major subcortical motor hubs including the internal pallidum (Neumann et al, 2015), the STN (Hirschmann et al, 2011;Litvak et al, 2011), the thalamus (Marsden et al, 2000) and the pedunculopontine nucleus (Jha et al, 2017). One influential account on physiological and pathophysiological beta activity may be summarized in the hypothesis that beta activity is related to the maintenance of the current cognitive or motor state (Engel and Fries, 2010).…”

Probabilistic conversion of neurosurgical DBS electrode coordinates into MNI space

“…This allows for direct conversion between each patient’s AC/PC coordinates and MNI coordinates. Indeed some neurosurgical studies are beginning to use this approach and report results in MNI space (Barow et al, 2014; Hohlefeld et al, 2015; Horn and Kühn, 2015; Merkl et al, 2015; 2013; Neumann et al, 2015a; 2015b; Riva-Posse et al, 2014; Schönecker et al, 2009; Schroll et al, 2015). However, these studies are few relative to the wealth of information in the neurosurigical literature.…”

Sensorimotor Integration and GABA-ergic Activity in Embouchure Dystonia: An Assessment with Magnetoencephalography

“…16 The increased alpha-, beta-, and gamma-band frequencies during dystonic activity implicate abnormal pallido-cerebellar and cortico-pallidal pathways. In another MEG study where sensory touch was used to stop dystonic activity, post-dystonic activity alpha and beta activities decreased, while gamma activity increased.…”