Neural signatures of hyperdirect pathway activity in Parkinson’s disease

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, Patricia Limousin, Rafal Bogacz, Bomin Sun, Masud Husain, Peter Brown () and Vladimir Litvak ()
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Ashwini Oswal: University of Oxford
Chunyan Cao: Shanghai JiaoTong University
Chien-Hung Yeh: University of Oxford
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
Bomin Sun: Shanghai JiaoTong University
Masud Husain: University of Oxford
Peter Brown: University of Oxford
Vladimir Litvak: University College London

Nature Communications, 2021, vol. 12, issue 1, 1-14

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-25366-0

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