Prisca Hsu, Cecilia Jobst, Silvia L. Isabella, Trish Domi, Robyn Westmacott, Nomazulu Dlamini, Douglas Cheyne
{"title":"Cortical Oscillatory Activity and Motor Control in Pediatric Stroke Patients With Hemidystonia","authors":"Prisca Hsu, Cecilia Jobst, Silvia L. Isabella, Trish Domi, Robyn Westmacott, Nomazulu Dlamini, Douglas Cheyne","doi":"10.1002/hbm.70204","DOIUrl":null,"url":null,"abstract":"<p>Dystonia is a movement disorder characterized by repetitive muscle contractions, twisting movements, and abnormal posture, affecting 20% of pediatric arterial ischemic stroke (AIS) survivors. Recent studies have reported that children with dystonia are at higher risk of cognitive deficits. The connection between impaired motor outcomes and cognitive impairment in dystonia is not fully understood; dystonia might affect motor control alone, or it could also contribute to cognitive impairment through disruptions in higher-order motor processes. To assess the functional correlates underlying motor control in children with dystonia, we used magnetoencephalography (MEG) to measure frontal theta (4–8 Hz), motor beta (15–30 Hz), and sensorimotor gamma (60–90 Hz) activity during a “go”/“no-go” task. Beamformer-based source analysis was carried out on 19 post-stroke patients: nine with dystonia (mean age = 13.78, SD = 2.82, 8 females), 10 without dystonia (mean age = 12.90, SD = 3.54, 4 females), and 17 healthy controls (mean age = 12.82, SD = 2.72, 8 females). To evaluate inhibitory control, frontal theta activity was analyzed during correct “no-go” (successful withhold) trials. To assess motor execution and sensorimotor integration, movement time-locked beta and sensorimotor gamma activity were analyzed during correct “go” trials. Additionally, the Delis-Kaplan Executive Function System (DKEFS) color-word interference task was used as a non-motor, inhibitory control task to evaluate general cognitive inhibition abilities. During affected hand use, dystonia patients had higher “no-go” error rates (failed withhold) compared to all other groups. Dystonia patients also exhibited higher frontal theta power during correct withhold responses for both affected and unaffected hands compared to healthy controls. Furthermore, dystonia patients exhibited decreased movement-evoked gamma power and gamma peak frequency compared to non-dystonia patients and healthy controls. Movement-related beta desynchronization (ERD) activity was increased in non-dystonia patients for both hands compared to healthy participants. These results confirm that post-stroke dystonia is associated with impaired frontally mediated inhibitory control, as reflected by increased frontal theta power. Post-stroke dystonia patients also exhibited reduced motor gamma activity during movement, reflecting altered sensorimotor integration. The increased beta ERD activity in non-dystonia patients may suggest compensatory sensorimotor plasticity not observed in dystonia patients. These findings suggest that differences in motor outcomes in childhood stroke result from a combination of cognitive and motor deficits.</p>","PeriodicalId":13019,"journal":{"name":"Human Brain Mapping","volume":"46 5","pages":""},"PeriodicalIF":3.5000,"publicationDate":"2025-04-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1002/hbm.70204","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Human Brain Mapping","FirstCategoryId":"3","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/hbm.70204","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROIMAGING","Score":null,"Total":0}
引用次数: 0
Abstract
Dystonia is a movement disorder characterized by repetitive muscle contractions, twisting movements, and abnormal posture, affecting 20% of pediatric arterial ischemic stroke (AIS) survivors. Recent studies have reported that children with dystonia are at higher risk of cognitive deficits. The connection between impaired motor outcomes and cognitive impairment in dystonia is not fully understood; dystonia might affect motor control alone, or it could also contribute to cognitive impairment through disruptions in higher-order motor processes. To assess the functional correlates underlying motor control in children with dystonia, we used magnetoencephalography (MEG) to measure frontal theta (4–8 Hz), motor beta (15–30 Hz), and sensorimotor gamma (60–90 Hz) activity during a “go”/“no-go” task. Beamformer-based source analysis was carried out on 19 post-stroke patients: nine with dystonia (mean age = 13.78, SD = 2.82, 8 females), 10 without dystonia (mean age = 12.90, SD = 3.54, 4 females), and 17 healthy controls (mean age = 12.82, SD = 2.72, 8 females). To evaluate inhibitory control, frontal theta activity was analyzed during correct “no-go” (successful withhold) trials. To assess motor execution and sensorimotor integration, movement time-locked beta and sensorimotor gamma activity were analyzed during correct “go” trials. Additionally, the Delis-Kaplan Executive Function System (DKEFS) color-word interference task was used as a non-motor, inhibitory control task to evaluate general cognitive inhibition abilities. During affected hand use, dystonia patients had higher “no-go” error rates (failed withhold) compared to all other groups. Dystonia patients also exhibited higher frontal theta power during correct withhold responses for both affected and unaffected hands compared to healthy controls. Furthermore, dystonia patients exhibited decreased movement-evoked gamma power and gamma peak frequency compared to non-dystonia patients and healthy controls. Movement-related beta desynchronization (ERD) activity was increased in non-dystonia patients for both hands compared to healthy participants. These results confirm that post-stroke dystonia is associated with impaired frontally mediated inhibitory control, as reflected by increased frontal theta power. Post-stroke dystonia patients also exhibited reduced motor gamma activity during movement, reflecting altered sensorimotor integration. The increased beta ERD activity in non-dystonia patients may suggest compensatory sensorimotor plasticity not observed in dystonia patients. These findings suggest that differences in motor outcomes in childhood stroke result from a combination of cognitive and motor deficits.
期刊介绍:
Human Brain Mapping publishes peer-reviewed basic, clinical, technical, and theoretical research in the interdisciplinary and rapidly expanding field of human brain mapping. The journal features research derived from non-invasive brain imaging modalities used to explore the spatial and temporal organization of the neural systems supporting human behavior. Imaging modalities of interest include positron emission tomography, event-related potentials, electro-and magnetoencephalography, magnetic resonance imaging, and single-photon emission tomography. Brain mapping research in both normal and clinical populations is encouraged.
Article formats include Research Articles, Review Articles, Clinical Case Studies, and Technique, as well as Technological Developments, Theoretical Articles, and Synthetic Reviews. Technical advances, such as novel brain imaging methods, analyses for detecting or localizing neural activity, synergistic uses of multiple imaging modalities, and strategies for the design of behavioral paradigms and neural-systems modeling are of particular interest. The journal endorses the propagation of methodological standards and encourages database development in the field of human brain mapping.