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Task-related brain functional network reconfigurations relate to motor recovery in chronic subcortical stroke.

ABSTRACT: Stroke leads to both regional brain functional disruptions and network reorganization. However, how brain functional networks reconfigure as task demand increases in stroke patients and whether such reorganization at baseline would facilitate post-stroke motor recovery are largely unknown. To address this gap, brain functional connectivity (FC) were examined at rest and motor tasks in eighteen chronic subcortical stroke patients and eleven age-matched healthy controls. Stroke patients underwent a 2-week intervention using a motor imagery-assisted brain computer interface-based (MI-BCI) training with or without transcranial direct current stimulation (tDCS). Motor recovery was determined by calculating the changes of the upper extremity component of the Fugl-Meyer Assessment (FMA) score between pre- and post-intervention divided by the pre-intervention FMA score. The results suggested that as task demand increased (i.e., from resting to passive unaffected hand gripping and to active affected hand gripping), patients showed greater FC disruptions in cognitive networks including the default and dorsal attention networks. Compared to controls, patients had lower task-related spatial similarity in the somatomotor-subcortical, default-somatomotor, salience/ventral attention-subcortical and subcortical-subcortical connections, suggesting greater inefficiency in motor execution. Importantly, higher baseline network-specific FC strength (e.g., dorsal attention and somatomotor) and more efficient brain network reconfigurations (e.g., somatomotor and subcortical) from rest to active affected hand gripping at baseline were related to better future motor recovery. Our findings underscore the importance of studying functional network reorganization during task-free and task conditions for motor recovery prediction in stroke.

SUBMITTER: Cheng HJ

PROVIDER: S-EPMC8055891 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:ObjectiveMotor recovery after stroke depends on the integrity of ipsilesional motor circuits and interactions between the ipsilesional and contralesional hemispheres. In this sham-controlled randomized trial, we investigated whether noninvasive modulation of regional excitability of bilateral motor cortices in combination with physical and occupational therapy improves motor outcome after stroke.MethodsTwenty chronic stroke patients were randomly assigned to receive 5 consecutive sessions of either 1) bihemispheric transcranial direct current stimulation (tDCS) (anodal tDCS to upregulate excitability of ipsilesional motor cortex and cathodal tDCS to downregulate excitability of contralesional motor cortex) with simultaneous physical/occupational therapy or 2) sham stimulation with simultaneous physical/occupational therapy. Changes in motor impairment (Upper Extremity Fugl-Meyer) and motor activity (Wolf Motor Function Test) assessments were outcome measures while functional imaging parameters were used to identify neural correlates of motor improvement.ResultsThe improvement of motor function was significantly greater in the real stimulation group (20.7% in Fugl-Meyer and 19.1% in Wolf Motor Function Test scores) when compared to the sham group (3.2% in Fugl-Meyer and 6.0% in Wolf Motor Function Test scores). The effects outlasted the stimulation by at least 1 week. In the real-stimulation group, stronger activation of intact ipsilesional motor regions during paced movements of the affected limb were found postintervention whereas no significant activation changes were seen in the control group.ConclusionsThe combination of bihemispheric tDCS and peripheral sensorimotor activities improved motor functions in chronic stroke patients that outlasted the intervention period. This novel approach may potentiate cerebral adaptive processes that facilitate motor recovery after stroke.Classification of evidenceThis study provides Class I evidence that for adult patients with ischemic stroke treated at least 5 months after their first and only stroke, bihemispheric tDCS and simultaneous physical/occupational therapy given over 5 consecutive sessions significantly improves motor function as measured by the Upper Extremity Fugl-Meyer assessment (raw change treated 6.1 ± 3.4, sham 1.2 ± 1.0).

Project description:Promoting the recovery of motor function and optimizing rehabilitation strategies for stroke patients is closely associated with the challenge of individual prediction. To date, stroke research has identified critical pathophysiological neural underpinnings at the cellular level as well as with regard to network reorganization. However, in order to generate reliable readouts at the level of individual patients and thereby realize translation from bench to bedside, we are still in a need for innovative methods. The combined use of transcranial magnetic stimulation (TMS) and EEG has proven powerful to record both local and network responses at an individual's level. To elucidate the potential of TMS-EEG to assess motor recovery after stroke, we used neuronavigated TMS-EEG over ipsilesional primary motor cortex (M1) in 28 stroke patients in the first days after stroke. Twenty-five of these patients were reassessed after >3 months post-stroke. In the early post-stroke phase (6.7 ± 2.5 days), the TMS-evoked EEG responses featured two markedly different response morphologies upon TMS to ipsilesional M1. In the first group of patients, TMS elicited a differentiated and sustained EEG response with a series of deflections sequentially involving both hemispheres. This response type resembled the patterns of bilateral activation as observed in the healthy comparison group. By contrast, in a subgroup of severely affected patients, TMS evoked a slow and simplified local response. Quantifying the TMS-EEG responses in the time and time-frequency domain revealed that stroke patients exhibited slower and simple responses with higher amplitudes compared to healthy controls. Importantly, these patterns of activity changes after stroke were not only linked to the initial motor deficit, but also to motor recovery after >3 months post-stroke. Thus, the data revealed a substantial impairment of local effects as well as causal interactions within the motor network early after stroke. Additionally, for severely affected patients with absent motor evoked potentials and identical clinical phenotype, TMS-EEG provided differential response patterns indicative of the individual potential for recovery of function. Thereby, TMS-EEG extends the methodological repertoire in stroke research by allowing the assessment of individual response profiles.

Project description:Predicting whether a chronic stroke patient is likely to benefit from a specific intervention can help patients establish reasonable expectations. It also provides the basis for candidates selecting for the intervention. Recent convergent evidence supports the value of network-based approach for understanding the relationship between dysfunctional neural activity and motor deficits after stroke. In this study, we applied resting-state brain connectivity networks to investigate intervention-specific predictive biomarkers of motor improvement in 22 chronic stroke participants who received either combined action observation with EEG-guided robot-hand training (Neural Guided-Action Observation Group, n = 12, age: 34-68 years) or robot-hand training without action observation and EEG guidance (non-Neural Guided-text group, n = 10, age: 42-57 years). The robot hand in Neural Guided-Action Observation training was activated only when significant mu suppression (8-12 Hz) was detected from participant's EEG signals in ipsilesional hemisphere while it was randomly activated in non-Neural Guided-text training. Only the Neural Guided-Action Observation group showed a significant long-term improvement in their upper-limb motor functions (P < 0.5). In contrast, no significant training effect on the paretic motor functions was found in the non-Neural Guided-text group (P > 0.5). The results of brain connectivity estimated via EEG coherence showed that the pre-training interhemispheric connectivity of delta, theta, alpha and contralesional connectivity of beta were motor improvement related in the Neural Guided-Action Observation group. They can not only differentiate participants with good and poor recovery (interhemispheric delta: P = 0.047, Hedges' g = 1.409; interhemispheric theta: P = 0.046, Hedges' g = 1.333; interhemispheric alpha: P = 0.038, Hedges' g = 1.536; contralesional beta: P = 0.027, Hedges' g = 1.613) but also significantly correlated with post-training intervention gains (interhemispheric delta: r = -0.901, P < 0.05; interhemispheric theta: r = -0.702, P < 0.05; interhemispheric alpha: r = -0.641, P < 0.05; contralesional beta: r = -0.729, P < 0.05). In contrast, no EEG coherence was significantly correlated with intervention gains in the non-Neural Guided-text group (all Ps>0.05 ). Partial least square regression showed that the combination of pre-training interhemispheric and contralesional local connectivity could precisely predict intervention gains in the Neural Guided-Action Observation group with a strong correlation between predicted and observed intervention gains (r = 0.82 r=0.82 ) and between predicted and observed intervention outcomes (r = 0.90 r=0.90 ). In summary, EEG-based resting-state brain connectivity networks may serve clinical decision-making by offering an approach to predicting Neural Guided-Action Observation training-induced motor improvement.

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Task-related brain functional network reconfigurations relate to motor recovery in chronic subcortical stroke.

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