Motor imagery-based brain-computer interface rehabilitation programs enhance upper extremity performance and cortical activation in stroke patients

Abstract

Background: The most challenging aspect of rehabilitation is the repurposing of residual functional plasticity in stroke patients. To achieve this, numerous plasticity-based clinical rehabilitation programs have been developed. This study aimed to investigate the effects of motor imagery (MI)-based brain-computer interface (BCI) rehabilitation programs on upper extremity hand function in patients with chronic hemiplegia.

Design: A 2010 Consolidated Standards for Test Reports (CONSORT)-compliant randomized controlled trial.

Methods: Forty-six eligible stroke patients with upper limb motor dysfunction participated in the study, six of whom dropped out. The patients were randomly divided into a BCI group and a control group. The BCI group received BCI therapy and conventional rehabilitation therapy, while the control group received conventional rehabilitation only. The Fugl-Meyer Assessment of the Upper Extremity (FMA-UE) score was used as the primary outcome to evaluate upper extremity motor function. Additionally, functional magnetic resonance imaging (fMRI) scans were performed on all patients before and after treatment, in both the resting and task states. We measured the amplitude of low-frequency fluctuation (ALFF), regional homogeneity (ReHo), z conversion of ALFF (zALFF), and z conversion of ReHo (ReHo) in the resting state. The task state was divided into four tasks: left-hand grasping, right-hand grasping, imagining left-hand grasping, and imagining right-hand grasping. Finally, meaningful differences were assessed using correlation analysis of the clinical assessments and functional measures.

Results: A total of 40 patients completed the study, 20 in the BCI group and 20 in the control group. Task-related blood-oxygen-level-dependent (BOLD) analysis showed that when performing the motor grasping task with the affected hand, the BCI group exhibited significant activation in the ipsilateral middle cingulate gyrus, precuneus, inferior parietal gyrus, postcentral gyrus, middle frontal gyrus, superior temporal gyrus, and contralateral middle cingulate gyrus. When imagining a grasping task with the affected hand, the BCI group exhibited greater activation in the ipsilateral superior frontal gyrus (medial) and middle frontal gyrus after treatment. However, the activation of the contralateral superior frontal gyrus decreased in the BCI group relative to the control group. Resting-state fMRI revealed increased zALFF in multiple cerebral regions, including the contralateral precentral gyrus and calcarine and the ipsilateral middle occipital gyrus and cuneus, and decreased zALFF in the ipsilateral superior temporal gyrus in the BCI group relative to the control group. Increased zReHo in the ipsilateral cuneus and contralateral calcarine and decreased zReHo in the contralateral middle temporal gyrus, temporal pole, and superior temporal gyrus were observed post-intervention. According to the subsequent correlation analysis, the increase in the FMA-UE score showed a positive correlation with the mean zALFF of the contralateral precentral gyrus (r = 0.425, P < 0.05), the mean zReHo of the right cuneus (r = 0.399, P < 0.05).

Conclusion: In conclusion, BCI therapy is effective and safe for arm rehabilitation after severe poststroke hemiparesis. The correlation of the zALFF of the contralateral precentral gyrus and the zReHo of the ipsilateral cuneus with motor improvements suggested that these values can be used as prognostic measures for BCI-based stroke rehabilitation. We found that motor function was related to visual and spatial processing, suggesting potential avenues for refining treatment strategies for stroke patients.

Trial registration: The trial is registered in the Chinese Clinical Trial Registry (number ChiCTR2000034848, registered July 21, 2020).

Keywords: Brain–computer interface (BCI); Fugl–Meyer Assessment of the Upper Extremity (FMA-UE); Motor imagery (MI); Stroke rehabilitation; fMRI.

Fig. 1

Schematic of the fMRI block design paradigm. All subjects performed two sessions of four tasks (a motor execution with left hands, b motor execution with right hands; c motor imagery with left hands, d motor imagery with right hands). During fMRI scanning, participants were asked to perform two different block design paradigms. For the first session (motor execution), the subjects grasped and relaxed the corresponding hands according to the prompts on the screen at a frequency of 1 Hz. For the second session (motor imagery), the subjects imagined the corresponding hand movements according to the arrows. Each “ON” block lasted for 20 s (8 TR) with the left and right hand displayed pseudorandomly, with intervals with an “OFF” block lasting 7–9 scans of blank screen displayed pseudorandomly. A total of 101 volumes were acquired per session

Fig. 2

Group differences in brain activation area on task-state fMRI during motor execution with the affected hand. Warm tones represent greater brain activation in the BCI group than in the control group, while cold tones represent less brain activation in the BCI group than in the control group. The z value was the z-axis coordinate along the anterior–posterior axis referenced to a stereotaxic brain SPM152 template

Fig. 3

Group differences in brain activation area in task-state fMRI of motor imagery with the affected hand. Warm tones represent greater brain activation in the BCI group than in the control group, while cold tones represent less brain activation in the BCI group than in the control group. The z value was the z-axis coordinate along the anterior–posterior axis referenced to a stereotaxic brain SPM152 template

Fig. 4

Group differences in zALFF in the resting-state scan. Warm tones represent greater zALFF values in the BCI group than in the control group, while cold tones represent lower zALFF values in the BCI group than in the control group. The z value was the z-axis coordinate along the anterior–posterior axis referenced to a stereotaxic brain SPM152 template

Fig. 5

Group differences in zReHo in the resting-state scan. Warm tones represent greater zReHo values in the BCI group than in the control group, while cold tones represent lower zReHo values in the BCI group than in the control group. The z value was the z-axis coordinate along the anterior–posterior axis referenced to a stereotaxic brain SPM152 template

Fig. 6

Correlation analysis between zALFF/zReHo and FMA-UE gains. The zALFF values of the ipsilesional primary motor cortex showed a trend toward a positive correlation with increased FMA-UE score (A). The zReHo values of the contralesional cuneus showed a trend toward a positive correlation with increased FMA-UE score (B)