Motor learning leverages coordinated low-frequency cortico-basal ganglia activity to optimize motor preparation in humans with Parkinson’s disease
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...
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| Format: | Article |
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Frontiers Media S.A.
2025-05-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2025.1542493/full |
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| author | Kara N. Presbrey Kara N. Presbrey Kara N. Presbrey Thomas A. Wozny Thomas A. Wozny Kenneth H. Louie Kenneth H. Louie Simon Little Simon Little Philip A. Starr Philip A. Starr Reza Abbasi-Asl Reza Abbasi-Asl Doris D. Wang Doris D. Wang |
| author_facet | Kara N. Presbrey Kara N. Presbrey Kara N. Presbrey Thomas A. Wozny Thomas A. Wozny Kenneth H. Louie Kenneth H. Louie Simon Little Simon Little Philip A. Starr Philip A. Starr Reza Abbasi-Asl Reza Abbasi-Asl Doris D. Wang Doris D. Wang |
| author_sort | Kara N. Presbrey |
| collection | DOAJ |
| description | 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. |
| format | Article |
| id | doaj-art-57bce7d2ed1944f5be90e9721fbf9c76 |
| institution | DOAJ |
| issn | 1662-453X |
| language | English |
| publishDate | 2025-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj-art-57bce7d2ed1944f5be90e9721fbf9c762025-08-20T02:57:44ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2025-05-011910.3389/fnins.2025.15424931542493Motor learning leverages coordinated low-frequency cortico-basal ganglia activity to optimize motor preparation in humans with Parkinson’s diseaseKara N. Presbrey0Kara N. Presbrey1Kara N. Presbrey2Thomas A. Wozny3Thomas A. Wozny4Kenneth H. Louie5Kenneth H. Louie6Simon Little7Simon Little8Philip A. Starr9Philip A. Starr10Reza Abbasi-Asl11Reza Abbasi-Asl12Doris D. Wang13Doris D. Wang14Department of Neurological Surgery, University of California San Francisco, San Francisco, CA, United StatesDepartment of Neurology, University of California San Francisco, San Francisco, CA, United StatesWeill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco, San Francisco, CA, United StatesWeill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco, San Francisco, CA, United StatesWeill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, United StatesDepartment of Neurology, University of California San Francisco, San Francisco, CA, United StatesWeill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco, San Francisco, CA, United StatesWeill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, United StatesDepartment of Neurology, University of California San Francisco, San Francisco, CA, United StatesWeill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco, San Francisco, CA, United StatesWeill Institute for Neurosciences, University of California San Francisco, San Francisco, CA, United StatesLearning 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.https://www.frontiersin.org/articles/10.3389/fnins.2025.1542493/fullParkinson’s diseasemovement decodingfunctional connectivitysequencingmotor learningmotor planning |
| spellingShingle | Kara N. Presbrey Kara N. Presbrey Kara N. Presbrey Thomas A. Wozny Thomas A. Wozny Kenneth H. Louie Kenneth H. Louie Simon Little Simon Little Philip A. Starr Philip A. Starr Reza Abbasi-Asl Reza Abbasi-Asl Doris D. Wang Doris D. Wang Motor learning leverages coordinated low-frequency cortico-basal ganglia activity to optimize motor preparation in humans with Parkinson’s disease Frontiers in Neuroscience Parkinson’s disease movement decoding functional connectivity sequencing motor learning motor planning |
| title | Motor learning leverages coordinated low-frequency cortico-basal ganglia activity to optimize motor preparation in humans with Parkinson’s disease |
| title_full | Motor learning leverages coordinated low-frequency cortico-basal ganglia activity to optimize motor preparation in humans with Parkinson’s disease |
| title_fullStr | Motor learning leverages coordinated low-frequency cortico-basal ganglia activity to optimize motor preparation in humans with Parkinson’s disease |
| title_full_unstemmed | Motor learning leverages coordinated low-frequency cortico-basal ganglia activity to optimize motor preparation in humans with Parkinson’s disease |
| title_short | Motor learning leverages coordinated low-frequency cortico-basal ganglia activity to optimize motor preparation in humans with Parkinson’s disease |
| title_sort | motor learning leverages coordinated low frequency cortico basal ganglia activity to optimize motor preparation in humans with parkinson s disease |
| topic | Parkinson’s disease movement decoding functional connectivity sequencing motor learning motor planning |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2025.1542493/full |
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