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

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 Fasano, William D. Hutchison Wd, Andres M. Lozano, Milad Lankarany, Andrea A. Kühn and Luka Milosevic ()
Additional contact information
Leon A. Steiner: University Health Network
David Crompton: University Health Network
Srdjan Sumarac: University Health Network
Artur Vetkas: University Health Network
Jürgen Germann: University Health Network
Maximilian Scherer: University Health Network
Maria Justich: University Health Network
Alexandre Boutet: University of Toronto
Milos R. Popovic: University of Toronto
Mojgan Hodaie: University Health Network
Suneil K. Kalia: University Health Network
Alfonso Fasano: University Health Network
William D. Hutchison Wd: University Health Network
Andres M. Lozano: University Health Network
Milad Lankarany: University Health Network
Andrea A. Kühn: Charité-Universitätsmedizin Berlin
Luka Milosevic: University Health Network

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-47552-6

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