Subthalamic nucleus long-range synchronization—an independent hallmark of human Parkinson’s disease

Shay Moshel, Reuben R. Shamir, Aeyal Raz, Fernando R. de Noriega, Renana Eitan, Hagai Bergman, Zvi Israel

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35 Scopus citations

Abstract

Beta-band synchronous oscillations in the dorsolateral region of the subthalamic nucleus (STN) of human patients with Parkinson’s disease (PD) have been frequently reported. However, the correlation between STN oscillations and synchronization has not been thoroughly explored. The simultaneous recordings of 2390 multi-unit pairs recorded by two parallel microelectrodes (separated by fixed distance of 2mm, n = 72 trajectories with two electrode tracks <4mm STN span) in 57 PD patients undergoing STN deep brain stimulation surgery were analyzed. Automatic procedures were utilized to divide the STN into dorsolateral oscillatory and ventromedial non-oscillatory regions, and to quantify the intensity of STN oscillations and synchronicity. Finally, the synchronicity of simultaneously vs. non-simultaneously recorded pairs were compared using a shuffling procedure. Synchronization was observed predominately in the beta range and only between multi-unit pairs in the dorsolateral oscillatory region (n = 615). In paired recordings between sites in the dorsolateral and ventromedial (n = 548) and ventromedial-ventromedial region pairs (n = 1227), no synchronization was observed. Oscillation and synchronicity intensity decline along the STN dorsolateral-ventromedial axis suggesting a fuzzy border between the STN regions. Synchronization strength was significantly correlated to the oscillation power, but synchronization was no longer observed following shuffling. We conclude that STN long-range beta oscillatory synchronization is due to increased neuronal coupling in the Parkinsonian brain and does not merely reflect the outcome of oscillations at similar frequency. The neural synchronization in the dorsolateral (probably the motor domain) STN probably augments the pathological changes in firing rate and patterns of subthalamic neurons in PD patients.

Original languageEnglish
Article number79
JournalFrontiers in Systems Neuroscience
Volume7
DOIs
StatePublished - 2013
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2013, Moshel, Shamir, Raz, deNoriega, Eitan, Bergman and Israel.

Funding

This work was supported partially by the Vorst Family Foundation for Parkinson Research, by the Simone and Bernard Guttman chair of Brain Research, and the generous support of the Rosetrees and Dekker foundations (to Hagai Bergman) as well as by the ELSC post-doctorate fellowships to Shay Moshel and Reuben R. Shamir and the PATH and Bloom foundations of London to Zvi Israel. We would like to thank Prof. Y. Ritov for statistical advice and Dr. S. Freeman and E. Singer for help in scientific editing.

FundersFunder number
Bloom foundations of London
ELSC
Rosetrees and Dekker foundations
Simone and Bernard Guttman chair of Brain Research
Vorst Family Foundation for Parkinson Research
PATH

    Keywords

    • Deep brain stimulation
    • Oscillations
    • Parkinson’s disease
    • Subthalamic nucleus
    • Synchronization

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