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Neural signatures of hyperdirect pathway activity in Parkinson’s disease

Author

Listed:
  • Ashwini Oswal

    (University of Oxford
    University of Oxford
    University College London)

  • Chunyan Cao

    (Shanghai JiaoTong University)

  • Chien-Hung Yeh

    (University of Oxford
    University of Oxford
    Beijing Institute of Technology)

  • Wolf-Julian Neumann

    (Charité University)

  • James Gratwicke

    (University College London)

  • Harith Akram

    (University College London)

  • Andreas Horn

    (Charité University)

  • Dianyou Li

    (Shanghai JiaoTong University)

  • Shikun Zhan

    (Shanghai JiaoTong University)

  • Chao Zhang

    (Shanghai JiaoTong University)

  • Qiang Wang

    (Charité University)

  • Ludvic Zrinzo

    (University College London)

  • Tom Foltynie

    (University College London)

  • Patricia Limousin

    (University College London)

  • Rafal Bogacz

    (University of Oxford
    University of Oxford)

  • Bomin Sun

    (Shanghai JiaoTong University)

  • Masud Husain

    (University of Oxford)

  • Peter Brown

    (University of Oxford
    University of Oxford)

  • Vladimir Litvak

    (University College London)

Abstract

Parkinson’s disease (PD) is characterised by the emergence of beta frequency oscillatory synchronisation across the cortico-basal-ganglia circuit. The relationship between the anatomy of this circuit and oscillatory synchronisation within it remains unclear. We address this by combining recordings from human subthalamic nucleus (STN) and internal globus pallidus (GPi) with magnetoencephalography, tractography and computational modelling. Coherence between supplementary motor area and STN within the high (21–30 Hz) but not low (13-21 Hz) beta frequency range correlated with ‘hyperdirect pathway’ fibre densities between these structures. Furthermore, supplementary motor area activity drove STN activity selectively at high beta frequencies suggesting that high beta frequencies propagate from the cortex to the basal ganglia via the hyperdirect pathway. Computational modelling revealed that exaggerated high beta hyperdirect pathway activity can provoke the generation of widespread pathological synchrony at lower beta frequencies. These findings suggest a spectral signature and a pathophysiological role for the hyperdirect pathway in PD.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-25366-0
    DOI: 10.1038/s41467-021-25366-0
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    Cited by:

    1. 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.
    2. Wang, Zhizhi & Hu, Bing & Zhou, Weiting & Xu, Minbo & Wang, Dingjiang, 2023. "Hopf bifurcation mechanism analysis in an improved cortex-basal ganglia network with distributed delays: An application to Parkinson’s disease," Chaos, Solitons & Fractals, Elsevier, vol. 166(C).

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