Cortical Oscillatory Activity and Motor Control in Pediatric Stroke Patients With Hemidystonia

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.

Keywords: MEG; MRI; dystonia; executive function; inhibitory control; pediatric stroke; “go”/“no‐go”.

FIGURE 1

(A) The “go”/“no‐go” task. Participants were presented with either a “go” or “no‐go” cue. The “go” cue was a green square, which required them to press a wooden paddle (shown in B). The “no‐go” cue was a red square in which case they were instructed to withhold their movement. The cue was displayed for 250 ms followed by a white square stimulus mask that remained on the screen for 1400–1800 ms. Each recording consisted of an equal number of “go” and “no‐go” trials presented randomly. (B) MEG‐compatible response device used for the “go”/“no‐go” task, allowing dystonia patients to use single (top) or multiple digits, or their entire hand (depending on severity of dystonic symptoms) (bottom) to respond by depressing the wooden paddle, which detected movement onset using a fiber optic light trigger. All non‐dystonia patients and healthy participants used their index fingers to press on the response device.

FIGURE 2

(A) Incorrect “no‐go” rates across stroke patients (dystonia and non‐dystonia) when using their affected hand and unaffected hands, as well as healthy controls. “No‐go” rates were calculated as a percentage based on the number of “no‐go” errors divided by total number of trials (# trials = 100). Dystonic patients exhibited significantly higher “no‐go” errors compared to their unaffected hand, non‐dystonic patients, and healthy controls. (B) No significant differences were found for incorrect “go” trials, although healthy controls generally had fewer errors. (C) No significant differences were found for mean reaction times between groups. (D) Coefficient of variation (CV) based on reaction time. Higher CV indicates less consistent motor responses between trials. No significant differences were found between groups. *p < 0.05; **p < 0.01; ***p < 0.001.

FIGURE 3

(A) Comparison of task‐related theta power between groups. Higher change in theta power suggests higher cognitive effort to correctly inhibit movement. A significant difference was found between dystonic patients using either hand versus non‐dystonic patients using their affected hand. (B) Timecourse of total power minus average power within the theta band relative to “no‐go” cue onset. Shaded area represents the standard error of mean (SEM). (C) Time‐frequency plots of induced source activity (1–50 Hz) for peak locations in the middle frontal cortex (highlighted in red on the CIVET cortical surface of one healthy control), for correct “no‐go” trials. **p < 0.01.

FIGURE 4

(A) Percent change in ipsilateral (left panel) and contralateral (right panel) beta ERD power across groups. Dystonic patients exhibited significantly greater change in contralateral beta ERD power when using their unaffected hand compared to their affected hand and to healthy controls. (B) Timecourse of total power minus average power within the beta band relative to “go” cue onset for ipsilateral (left panel) and contralateral (right panel) beta ERD. Shaded area represents the SEM. (C) Time‐frequency plots of induced source activity (1–50 Hz) for peak locations in the ipsilateral (left panel) and contralateral (right panel) precentral cortex (highlighted in blue on the CIVET cortical surface of one healthy control) for correct “go” trials. *p < 0.05; ***p < 0.001.

FIGURE 5

(A) Percent change in ipsilateral (left panel) and contralateral (right panel) beta ERS power across groups. No statistically significant differences were found. (B) Timecourse of total power minus average power within the beta band relative to “go” cue onset for ipsilateral (left panel) and contralateral (right panel) beta ERS. Shading indicates SEM. (C) Time‐frequency plots of induced source activity (1–50 Hz) for peak locations in the ipsilateral (left panel) and contralateral (right panel) precentral cortex (highlighted in red on the CIVET cortical surface of one healthy control) for correct “go” trials.

FIGURE 6

(A) Comparison of gamma power between groups. Non‐dystonic patients exhibited significantly higher change in gamma power compared to dystonic patients when using their affected hands. (B) Comparison of gamma peak frequency across groups. Healthy controls exhibited significantly higher gamma peak frequency compared to dystonic patients when using their affected hand. (C) Time course of total power minus average power within the gamma band relative to “go” cue onset. Shading indicates SEM. (D) TFRs of induced source activity (60–90 Hz) for peak locations in the contralateral precentral cortex (highlighted in red on the CIVET cortical surface of one healthy control) during correct “go” responses. *p < 0.05.