Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor control
Abstract Increasing evidence suggests a considerable role of pre-movement beta bursts for motor control and its impairment in Parkinson’s disease. However, whether beta bursts occur during precise and prolonged movements and if they affect fine motor control remains unclear. To investigate the role...
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2024-04-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-47555-3 |
| _version_ | 1797209241487933440 |
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| author | Manuel Bange Gabriel Gonzalez-Escamilla Damian M. Herz Gerd Tinkhauser Martin Glaser Dumitru Ciolac Alek Pogosyan Svenja L. Kreis Heiko J. Luhmann Huiling Tan Sergiu Groppa |
| author_facet | Manuel Bange Gabriel Gonzalez-Escamilla Damian M. Herz Gerd Tinkhauser Martin Glaser Dumitru Ciolac Alek Pogosyan Svenja L. Kreis Heiko J. Luhmann Huiling Tan Sergiu Groppa |
| author_sort | Manuel Bange |
| collection | DOAJ |
| description | Abstract Increasing evidence suggests a considerable role of pre-movement beta bursts for motor control and its impairment in Parkinson’s disease. However, whether beta bursts occur during precise and prolonged movements and if they affect fine motor control remains unclear. To investigate the role of within-movement beta bursts for fine motor control, we here combine invasive electrophysiological recordings and clinical deep brain stimulation in the subthalamic nucleus in 19 patients with Parkinson’s disease performing a context-varying task that comprised template-guided and free spiral drawing. We determined beta bursts in narrow frequency bands around patient-specific peaks and assessed burst amplitude, duration, and their immediate impact on drawing speed. We reveal that beta bursts occur during the execution of drawing movements with reduced duration and amplitude in comparison to rest. Exclusively when drawing freely, they parallel reductions in acceleration. Deep brain stimulation increases the acceleration around beta bursts in addition to a general increase in drawing velocity and improvements of clinical function. These results provide evidence for a diverse and task-specific role of subthalamic beta bursts for fine motor control in Parkinson’s disease; suggesting that pathological beta bursts act in a context dependent manner, which can be targeted by clinical deep brain stimulation. |
| first_indexed | 2024-04-24T09:51:34Z |
| format | Article |
| id | doaj.art-e18b26b7de694c38b58514713079f984 |
| institution | Directory Open Access Journal |
| issn | 2041-1723 |
| language | English |
| last_indexed | 2024-04-24T09:51:34Z |
| publishDate | 2024-04-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Nature Communications |
| spelling | doaj.art-e18b26b7de694c38b58514713079f9842024-04-14T11:21:22ZengNature PortfolioNature Communications2041-17232024-04-0115111510.1038/s41467-024-47555-3Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor controlManuel Bange0Gabriel Gonzalez-Escamilla1Damian M. Herz2Gerd Tinkhauser3Martin Glaser4Dumitru Ciolac5Alek Pogosyan6Svenja L. Kreis7Heiko J. Luhmann8Huiling Tan9Sergiu Groppa10Section of Movement Disorders and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg-University MainzSection of Movement Disorders and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg-University MainzSection of Movement Disorders and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg-University MainzDepartment of Neurology, Bern University Hospital and University of BernDepartment of Neurosurgery, University Medical Center of the Johannes Gutenberg-University MainzSection of Movement Disorders and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg-University MainzMRC Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of OxfordInstitute of Physiology, University Medical Center of the Johannes Gutenberg-University MainzInstitute of Physiology, University Medical Center of the Johannes Gutenberg-University MainzMRC Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of OxfordSection of Movement Disorders and Neurostimulation, Department of Neurology, Focus Program Translational Neuroscience (FTN), University Medical Center of the Johannes Gutenberg-University MainzAbstract Increasing evidence suggests a considerable role of pre-movement beta bursts for motor control and its impairment in Parkinson’s disease. However, whether beta bursts occur during precise and prolonged movements and if they affect fine motor control remains unclear. To investigate the role of within-movement beta bursts for fine motor control, we here combine invasive electrophysiological recordings and clinical deep brain stimulation in the subthalamic nucleus in 19 patients with Parkinson’s disease performing a context-varying task that comprised template-guided and free spiral drawing. We determined beta bursts in narrow frequency bands around patient-specific peaks and assessed burst amplitude, duration, and their immediate impact on drawing speed. We reveal that beta bursts occur during the execution of drawing movements with reduced duration and amplitude in comparison to rest. Exclusively when drawing freely, they parallel reductions in acceleration. Deep brain stimulation increases the acceleration around beta bursts in addition to a general increase in drawing velocity and improvements of clinical function. These results provide evidence for a diverse and task-specific role of subthalamic beta bursts for fine motor control in Parkinson’s disease; suggesting that pathological beta bursts act in a context dependent manner, which can be targeted by clinical deep brain stimulation.https://doi.org/10.1038/s41467-024-47555-3 |
| spellingShingle | Manuel Bange Gabriel Gonzalez-Escamilla Damian M. Herz Gerd Tinkhauser Martin Glaser Dumitru Ciolac Alek Pogosyan Svenja L. Kreis Heiko J. Luhmann Huiling Tan Sergiu Groppa Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor control Nature Communications |
| title | Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor control |
| title_full | Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor control |
| title_fullStr | Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor control |
| title_full_unstemmed | Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor control |
| title_short | Subthalamic stimulation modulates context-dependent effects of beta bursts during fine motor control |
| title_sort | subthalamic stimulation modulates context dependent effects of beta bursts during fine motor control |
| url | https://doi.org/10.1038/s41467-024-47555-3 |
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