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Neural signatures of indirect pathway activity during subthalamic stimulation in Parkinson’s disease

Author

Listed:
  • Leon A. Steiner

    (University Health Network
    Charité-Universitätsmedizin Berlin
    Berlin Institute of Health (BIH))

  • David Crompton

    (University Health Network
    University of Toronto)

  • Srdjan Sumarac

    (University Health Network
    University of Toronto)

  • Artur Vetkas

    (University Health Network
    Toronto Western Hospital)

  • Jürgen Germann

    (University Health Network
    Toronto Western Hospital
    University of Toronto)

  • Maximilian Scherer

    (University Health Network
    University of Toronto)

  • Maria Justich

    (University Health Network
    University of Toronto
    Toronto Western Hospital)

  • Alexandre Boutet

    (University of Toronto)

  • Milos R. Popovic

    (University of Toronto
    University Health Network
    Center for Advancing Neurotechnological Innovation to Application (CRANIA))

  • Mojgan Hodaie

    (University Health Network
    Toronto Western Hospital
    University of Toronto
    Center for Advancing Neurotechnological Innovation to Application (CRANIA))

  • Suneil K. Kalia

    (University Health Network
    Toronto Western Hospital
    University of Toronto
    University Health Network)

  • Alfonso Fasano

    (University Health Network
    University of Toronto
    Toronto Western Hospital
    Center for Advancing Neurotechnological Innovation to Application (CRANIA))

  • William D. Hutchison WD

    (University Health Network
    University of Toronto
    Center for Advancing Neurotechnological Innovation to Application (CRANIA)
    University of Toronto)

  • Andres M. Lozano

    (University Health Network
    Toronto Western Hospital
    University of Toronto
    Center for Advancing Neurotechnological Innovation to Application (CRANIA))

  • Milad Lankarany

    (University Health Network
    University of Toronto
    Center for Advancing Neurotechnological Innovation to Application (CRANIA))

  • Andrea A. Kühn

    (Charité-Universitätsmedizin Berlin)

  • Luka Milosevic

    (University Health Network
    University of Toronto
    University Health Network
    Center for Advancing Neurotechnological Innovation to Application (CRANIA))

Abstract

Deep brain stimulation (DBS) of the subthalamic nucleus (STN) produces an electrophysiological signature called evoked resonant neural activity (ERNA); a high-frequency oscillation that has been linked to treatment efficacy. However, the single-neuron and synaptic bases of ERNA are unsubstantiated. This study proposes that ERNA is a subcortical neuronal circuit signature of DBS-mediated engagement of the basal ganglia indirect pathway network. In people with Parkinson’s disease, we: (i) showed that each peak of the ERNA waveform is associated with temporally-locked neuronal inhibition in the STN; (ii) characterized the temporal dynamics of ERNA; (iii) identified a putative mesocircuit architecture, embedded with empirically-derived synaptic dynamics, that is necessary for the emergence of ERNA in silico; (iv) localized ERNA to the dorsal STN in electrophysiological and normative anatomical space; (v) used patient-wise hotspot locations to assess spatial relevance of ERNA with respect to DBS outcome; and (vi) characterized the local fiber activation profile associated with the derived group-level ERNA hotspot.

Suggested Citation

  • Leon A. Steiner & David Crompton & Srdjan Sumarac & Artur Vetkas & Jürgen Germann & Maximilian Scherer & Maria Justich & Alexandre Boutet & Milos R. Popovic & Mojgan Hodaie & Suneil K. Kalia & Alfonso, 2024. "Neural signatures of indirect pathway activity during subthalamic stimulation in Parkinson’s disease," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47552-6
    DOI: 10.1038/s41467-024-47552-6
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    References listed on IDEAS

    as
    1. Brice Crompe & Asier Aristieta & Arthur Leblois & Salma Elsherbiny & Thomas Boraud & Nicolas P. Mallet, 2020. "Publisher Correction: The globus pallidus orchestrates abnormal network dynamics in a model of Parkinsonism," Nature Communications, Nature, vol. 11(1), pages 1-1, December.
    2. Brice de la Crompe & Asier Aristieta & Arthur Leblois & Salma Elsherbiny & Thomas Boraud & Nicolas P. Mallet, 2020. "The globus pallidus orchestrates abnormal network dynamics in a model of Parkinsonism," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    3. Ashwini Oswal & Chunyan Cao & Chien-Hung Yeh & Wolf-Julian Neumann & James Gratwicke & Harith Akram & Andreas Horn & Dianyou Li & Shikun Zhan & Chao Zhang & Qiang Wang & Ludvic Zrinzo & Tom Foltynie &, 2021. "Neural signatures of hyperdirect pathway activity in Parkinson’s disease," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
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    Cited by:

    1. Varvara Mathiopoulou & Jeroen Habets & Lucia K. Feldmann & Johannes L. Busch & Jan Roediger & Jennifer K. Behnke & Gerd-Helge Schneider & Katharina Faust & Andrea A. Kühn, 2025. "Gamma entrainment induced by deep brain stimulation as a biomarker for motor improvement with neuromodulation," Nature Communications, Nature, vol. 16(1), pages 1-11, December.
    2. Nicola Ria & Ahmed Eladly & Eduard Masvidal-Codina & Xavi Illa & Anton Guimerà & Kate Hills & Ramon Garcia-Cortadella & Fikret Taygun Duvan & Samuel M. Flaherty & Michal Prokop & Rob. C. Wykes & Kosta, 2025. "Flexible graphene-based neurotechnology for high-precision deep brain mapping and neuromodulation in Parkinsonian rats," Nature Communications, Nature, vol. 16(1), pages 1-16, December.

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