Cortico-pallidal oscillatory connectivity in patients with dystonia.
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.
1 Department of Neurology, Campus Virchow Klinikum, Charité-University Medicine Berlin, Augustenburger Platz 1,13353 Berlin, Germany 2 The Wellcome Trust Centre for Neuroimaging, UCL Institute of Neurology, 12 Queen Square, London WC1N 3BG, UK.
Wolf-Julian
WJ
Neumann
3 Sobell Department of Movement Disorders, UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK.
Ashwani
A
Jha
1 Department of Neurology, Campus Virchow Klinikum, Charité-University Medicine Berlin, Augustenburger Platz 1,13353 Berlin, Germany.
Antje
A
Bock
1 Department of Neurology, Campus Virchow Klinikum, Charité-University Medicine Berlin, Augustenburger Platz 1,13353 Berlin, Germany.
Julius
J
Huebl
1 Department of Neurology, Campus Virchow Klinikum, Charité-University Medicine Berlin, Augustenburger Platz 1,13353 Berlin, Germany.
Andreas
A
Horn
4 Department of Neurosurgery, Campus Virchow Klinikum, Charité-University Medicine Berlin, Augustenburger Platz 1,13353 Berlin, Germany.
Gerd-Helge
GH
Schneider
5 Physikalisch-Technische Bundesanstalt, Institut Berlin, Abbestr. 2-12, 10587 Berlin, Germany.
Tillmann H
TH
Sander
2 The Wellcome Trust Centre for Neuroimaging, UCL Institute of Neurology, 12 Queen Square, London WC1N 3BG, UK.
Vladimir
V
Litvak
1 Department of Neurology, Campus Virchow Klinikum, Charité-University Medicine Berlin, Augustenburger Platz 1,13353 Berlin, Germany 6 Berlin School of Mind and Brain, Charité - University Medicine Berlin, Unter den Linden 6, 10099 Berlin,Germany Berlin, Germany 7 NeuroCure, Charité - University Medicine Berlin, Charitéplatz 1, 10117 Berlin, Germany andrea.kuehn@charite.de.
Andrea A
AA
Kühn
D000328:Adult; D002531:Cerebellum / Q000503:physiopathology*; D046690:Deep Brain Stimulation; D020821:Dystonic Disorders / Q000503:physiopathology* / Q000628:therapy; D005260:Female; D005917:Globus Pallidus / Q000503:physiopathology*; D006801:Humans; D015225:Magnetoencephalography / Q000379:methods*; D008297:Male; D008875:Middle Aged; D009434:Neural Pathways / Q000503:physiopathology*; D013702:Temporal Lobe / Q000503:physiopathology*; D055815:Young Adult
deep brain stimulation; dystonia; globus pallidus internus; magnetoencephalography; oscillations