Subthalamic stimulation modulates cortical motor network activity and synchronization in Parkinson’s disease
| Autor: | Daniel Weiss, Marlieke Scholten, Georgios Naros, Alireza Gharabaghi, Ander Ramos-Murguialday, Friedemann Bunjes, Rejko Krüger, Rosa Klotz, Rathinaswamy B. Govindan, Christian Plewnia, Christoph Meisner |
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| Rok vydání: | 2015 |
| Předmět: |
Male
therapy [Parkinson Disease] Time Factors Deep Brain Stimulation medicine.medical_treatment Stimulation Antiparkinson Agents Levodopa physiology [Subthalamus] 0302 clinical medicine physiology [Cortical Synchronization] Neural Pathways physiopathology [Nerve Net] Longitudinal Studies Cortical Synchronization 0303 health sciences Motor Cortex Subthalamus Parkinson Disease Middle Aged Subthalamic nucleus Treatment Outcome medicine.anatomical_structure Female drug effects [Psychomotor Performance] Psychology Motor cortex Adult Deep brain stimulation Motor program therapeutic use [Levodopa] physiology [Evoked Potentials Motor] 03 medical and health sciences methods [Deep Brain Stimulation] medicine drug effects [Cortical Synchronization] Humans ddc:610 Aged therapeutic use [Antiparkinson Agents] 030304 developmental biology physiopathology [Neural Pathways] physiopathology [Motor Cortex] Original Articles Evoked Potentials Motor Phase synchronization pathology [Parkinson Disease] Neurology (clinical) Nerve Net Neuroscience Psychomotor Performance 030217 neurology & neurosurgery |
| Zdroj: | Brain Brain 138(3), 679-693 (2015). doi:10.1093/brain/awu380 |
| ISSN: | 1460-2156 0006-8950 |
| DOI: | 10.1093/brain/awu380 |
| Popis: | Dynamic modulations of large-scale network activity and synchronization are inherent to a broad spectrum of cognitive processes and are disturbed in neuropsychiatric conditions including Parkinson's disease. Here, we set out to address the motor network activity and synchronization in Parkinson's disease and its modulation with subthalamic stimulation. To this end, 20 patients with idiopathic Parkinson's disease with subthalamic nucleus stimulation were analysed on externally cued right hand finger movements with 1.5-s interstimulus interval. Simultaneous recordings were obtained from electromyography on antagonistic muscles (right flexor digitorum and extensor digitorum) together with 64-channel electroencephalography. Time-frequency event-related spectral perturbations were assessed to determine cortical and muscular activity. Next, cross-spectra in the time-frequency domain were analysed to explore the cortico-cortical synchronization. The time-frequency modulations enabled us to select a time-frequency range relevant for motor processing. On these time-frequency windows, we developed an extension of the phase synchronization index to quantify the global cortico-cortical synchronization and to obtain topographic differentiations of distinct electrode sites with respect to their contributions to the global phase synchronization index. The spectral measures were used to predict clinical and reaction time outcome using regression analysis. We found that movement-related desynchronization of cortical activity in the upper alpha and beta range was significantly facilitated with 'stimulation on' compared to 'stimulation off' on electrodes over the bilateral parietal, sensorimotor, premotor, supplementary-motor, and prefrontal areas, including the bilateral inferior prefrontal areas. These spectral modulations enabled us to predict both clinical and reaction time improvement from subthalamic stimulation. With 'stimulation on', interhemispheric cortico-cortical coherence in the beta band was significantly attenuated over the bilateral sensorimotor areas. Similarly, the global cortico-cortical phase synchronization was attenuated, and the topographic differentiation revealed stronger desynchronization over the (ipsilateral) right-hemispheric prefrontal, premotor and sensorimotor areas compared to 'stimulation off'. We further demonstrated that the cortico-cortical phase synchronization was largely dominated by genuine neuronal coupling. The clinical improvement with 'stimulation on' compared to 'stimulation off' could be predicted from this cortical decoupling with multiple regressions, and the reduction of synchronization over the right prefrontal area showed a linear univariate correlation with clinical improvement. Our study demonstrates wide-spread activity and synchronization modulations of the cortical motor network, and highlights subthalamic stimulation as a network-modulating therapy. Accordingly, subthalamic stimulation may release bilateral cortical computational resources by facilitating movement-related desynchronization. Moreover, the subthalamic nucleus is critical to balance inhibitory and facilitatory cortical players within the motor program. |
| Databáze: | OpenAIRE |
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