ORIGINAL RESEARCH article
Front. Neurosci.
Sec. Translational Neuroscience
Volume 19 - 2025 | doi: 10.3389/fnins.2025.1542493
Motor learning leverages coordinated low-frequency cortico-basal ganglia activity to optimize motor preparation in humans with Parkinson's Disease
Provisionally accepted
- University of California, San Francisco, San Francisco, United States
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Learning dexterous motor sequences is crucial to autonomy and quality of life but can be altered in Parkinson’s Disease (PD). Learning involves optimizing pre-movement planning (preplanning) of multiple sequence elements to reduce computational overhead during active movement. However, it is unclear which brain regions mediate preplanning or how this process evolves with learning. Recording cortico-basal ganglia field potentials during a multi-day typing task in four individuals with PD, we found evidence for network-wide multi-element preplanning that improved with learning, facilitated by functional connectivity. In both cortex and basal ganglia, pre-movement gamma (γ, 30-250 Hz) activity, historically linked to population spiking, distinguished between future action sequences and became increasingly predictive with learning. For motor cortex γ, this increase was tied to learning-related cross-frequency coupling led by cortically-driven network delta (δ, 0.5-4 Hz) synchrony. More generally, coordinated network δ supported a complex pattern of learning-driven cross-frequency couplings within and between cortex and basal ganglia, including striatal lead of cortical beta (β, 12-30 Hz) activity, reflecting the specialized roles of these brain regions in motor preparation. In contrast, impaired learning was characterized by practice-driven decreases in γ’s predictive value, limited cross-frequency coupling and absent network δ synchrony, with network dynamics possibly altered by pathologically high inter-basal ganglia δ synchrony. These results suggest that cortically-led δ phase coordination optimized cortico-basal ganglia multi-element preplanning through enhanced recruitment of higher-frequency neural activity. Neurostimulation that enhances cortico-basal ganglia δ synchrony may thus hold potential for improving skilled fine motor control in PD.
Keywords: Parkinson's disease, movement decoding, functional connectivity, Sequencing, motor learning, Motor planning, fine motor control, hierarchical networks
Received: 09 Dec 2024; Accepted: 28 Apr 2025.
Copyright: © 2025 Presbrey, Wozny, Louie, Little, Starr, Abbasi-Asl and Wang. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
* Correspondence: Kara N Presbrey, University of California, San Francisco, San Francisco, United States
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