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Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor control

Author

Listed:
  • Manuel Bange

    (University Medical Center of the Johannes Gutenberg-University Mainz)

  • Gabriel Gonzalez-Escamilla

    (University Medical Center of the Johannes Gutenberg-University Mainz)

  • Damian M. Herz

    (University Medical Center of the Johannes Gutenberg-University Mainz
    University of Oxford)

  • Gerd Tinkhauser

    (Bern University Hospital and University of Bern)

  • Martin Glaser

    (University Medical Center of the Johannes Gutenberg-University Mainz)

  • Dumitru Ciolac

    (University Medical Center of the Johannes Gutenberg-University Mainz)

  • Alek Pogosyan

    (University of Oxford)

  • Svenja L. Kreis

    (University Medical Center of the Johannes Gutenberg-University Mainz)

  • Heiko J. Luhmann

    (University Medical Center of the Johannes Gutenberg-University Mainz)

  • Huiling Tan

    (University of Oxford)

  • Sergiu Groppa

    (University Medical Center of the Johannes Gutenberg-University Mainz)

Abstract

Increasing evidence suggests a considerable role of pre-movement beta bursts for motor control and its impairment in Parkinson’s disease. However, whether beta bursts occur during precise and prolonged movements and if they affect fine motor control remains unclear. To investigate the role of within-movement beta bursts for fine motor control, we here combine invasive electrophysiological recordings and clinical deep brain stimulation in the subthalamic nucleus in 19 patients with Parkinson’s disease performing a context-varying task that comprised template-guided and free spiral drawing. We determined beta bursts in narrow frequency bands around patient-specific peaks and assessed burst amplitude, duration, and their immediate impact on drawing speed. We reveal that beta bursts occur during the execution of drawing movements with reduced duration and amplitude in comparison to rest. Exclusively when drawing freely, they parallel reductions in acceleration. Deep brain stimulation increases the acceleration around beta bursts in addition to a general increase in drawing velocity and improvements of clinical function. These results provide evidence for a diverse and task-specific role of subthalamic beta bursts for fine motor control in Parkinson’s disease; suggesting that pathological beta bursts act in a context dependent manner, which can be targeted by clinical deep brain stimulation.

Suggested Citation

  • Manuel Bange & Gabriel Gonzalez-Escamilla & Damian M. Herz & Gerd Tinkhauser & Martin Glaser & Dumitru Ciolac & Alek Pogosyan & Svenja L. Kreis & Heiko J. Luhmann & Huiling Tan & Sergiu Groppa, 2024. "Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor control," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47555-3
    DOI: 10.1038/s41467-024-47555-3
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    References listed on IDEAS

    as
    1. Damian M. Herz & Manuel Bange & Gabriel Gonzalez-Escamilla & Miriam Auer & Keyoumars Ashkan & Petra Fischer & Huiling Tan & Rafal Bogacz & Muthuraman Muthuraman & Sergiu Groppa & Peter Brown, 2022. "Dynamic control of decision and movement speed in the human basal ganglia," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    3. Benoit Duchet & Filippo Ghezzi & Gihan Weerasinghe & Gerd Tinkhauser & Andrea A Kühn & Peter Brown & Christian Bick & Rafal Bogacz, 2021. "Average beta burst duration profiles provide a signature of dynamical changes between the ON and OFF medication states in Parkinson’s disease," PLOS Computational Biology, Public Library of Science, vol. 17(7), pages 1-42, July.
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