Differential modulation of STN-cortical and cortico-muscular coherence by movement and levodopa in Parkinson's disease

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Abstract

Previous research suggests that oscillatory coupling between cortex, basal ganglia and muscles plays an important role in motor behavior. Furthermore, there is evidence that oscillatory coupling is altered in patients with movement disorders such as Parkinson's disease (PD).

In this study, we performed simultaneous magnetoencephalography (MEG), local field potential (LFP) and electromyogram (EMG) recordings in PD patients selected for therapeutic subthalamic nucleus (STN) stimulation. Patients were recorded (i) after withdrawal of anti-parkinsonian medication (OFF) and (ii) after levodopa administration (ON). We analyzed STN-cortical and cortico-muscular coherence during static forearm contraction and repetitive hand movement in order to evaluate modulations of coherence by movement and medication. Based on previous results from studies investigating resting state coherence in PD patients, we selected primary motor cortex (M1) and superior temporal gyrus (STG) as regions of interest.

We found beta coherence between M1 and STN to be suppressed by administration of levodopa. M1–muscular coherence was strongly reduced in the alpha and beta band during repetitive movement compared to static contraction, but was unaffected by administration of levodopa. Strong STG–STN but not STG–muscular coherence could be observed in the alpha band. Coherence with STG was modulated neither by movement nor by medication. Finally, we found both M1–STN and M1–muscular beta coherence to be negatively correlated with UPDRS akinesia and rigidity sub-scores in the OFF state.

The present study provides new insights into the functional roles of STN-cortical and cortico-muscular coherence and their relationship to PD symptoms. The results indicate that STN-cortical and cortico-muscular coupling are correlated, but can be modulated independently. Moreover, they show differences in their frequency-specific topography. We conclude that they represent partly independent sub-loops within the motor system. Given their negative correlation with akinesia, neither can be considered “antikinetic”.

Highlights

▸ Administration of levodopa reduced M1–STN beta coherence. ▸ Repetitive movement reduced alpha and beta M1–muscular coherence. ▸ STN but not muscle coherent to superior temporal gyrus in alpha band ▸ M1–STN and M1–muscular beta coherence anti-correlated with akinesia in OFF state

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