Brain Functional Networks Study of Subacute Stroke Patients With Upper Limb Dysfunction After Comprehensive Rehabilitation Including BCI Training

Abstract

Brain computer interface (BCI)-based training is promising for the treatment of stroke patients with upper limb (UL) paralysis. However, most stroke patients receive comprehensive treatment that not only includes BCI, but also routine training. The purpose of this study was to investigate the topological alterations in brain functional networks following comprehensive treatment, including BCI training, in the subacute stage of stroke. Twenty-five hospitalized subacute stroke patients with moderate to severe UL paralysis were assigned to one of two groups: 4-week comprehensive treatment, including routine and BCI training (BCI group, BG, n = 14) and 4-week routine training without BCI support (control group, CG, n = 11). Functional UL assessments were performed before and after training, including, Fugl-Meyer Assessment-UL (FMA-UL), Action Research Arm Test (ARAT), and Wolf Motor Function Test (WMFT). Neuroimaging assessment of functional connectivity (FC) in the BG was performed by resting state functional magnetic resonance imaging. After training, as compared with baseline, all clinical assessments (FMA-UL, ARAT, and WMFT) improved significantly (p < 0.05) in both groups. Meanwhile, better functional improvements were observed in FMA-UL (p < 0.05), ARAT (p < 0.05), and WMFT (p < 0.05) in the BG. Meanwhile, FC of the BG increased across the whole brain, including the temporal, parietal, and occipital lobes and subcortical regions. More importantly, increased inter-hemispheric FC between the somatosensory association cortex and putamen was strongly positively associated with UL motor function after training. Our findings demonstrate that comprehensive rehabilitation, including BCI training, can enhance UL motor function better than routine training for subacute stroke patients. The reorganization of brain functional networks topology in subacute stroke patients allows for increased coordination between the multi-sensory and motor-related cortex and the extrapyramidal system. Future long-term, longitudinal, controlled neuroimaging studies are needed to assess the effectiveness of BCI training as an approach to promote brain plasticity during the subacute stage of stroke.

Keywords: brain computer interface; functional connectivity; neural plasticity; resting state functional magnetic resonance imaging; stroke.

Figure 1

Schematic Diagram of the BCI Training System. During BCI training sessions, patients imagine the movement of affected UL to desynchronize the sensorimotor rhythm. If the mu suppression score was below the threshold, the exoskeleton hand would move.

Figure 2

Combined Brain Atlas of the Brodmann Atlas and AAL. Brain atlas was constructed by appending the cerebellum mapping in AAL to the Brodmann atlas. Each colored area presents a functional node in the brain network. This illustration was visualized using BrainNet Viewer (https://www.nitrc.org/projects/bnv/).

Figure 3

Relationship between Clinical Scores and Functional Alterations. Graphical abstract of this study, patients were assigned to one of BG and CG. Functional assessments of both groups and FC in the BG were performed before and after 4 weeks training. Relationship of FC and clinical scores were analyzed in BG.

Figure 4

Position of Putamen and BA48. Position of BA48 had a center position on MNI: −38, 1, 13 in this study. Each colored area presents a functional node. This screenshot was captured using MRIcron (https://www.nitrc.org/projects/mricron).

Figure 5

Schematic Diagram of Increased FC in the BG. Red lines represent significantly increased inter- and intra-hemispheric FCs, L, left hemisphere; R, right hemisphere.

Figure 6

Significance of FC Changes in the BG. Red points and yellow points indicate the significance of FC change in the BG. BA2, BA3, primary somatosensory cortex; BA4, primary motor cortex; BA5, somatosensory association cortex; BA6, Premotor Cortex; BA7, superior parietal lobule; BA41, Primary Auditory Cortex; BA37, lateral occipitotemporal cortex; BA19, associative visual cortex; BA48, putamen; BA44, pars opercularis.

Figure 7

Correlation between FC and FMA-UL_post score of the BG. Increases in FC between the left BA5 and the right BA48 were positively correlated with FMA-UL_post score after training in the BG. FC (BA5L-BA48R): FC between the left somatosensory association cortex and the right putamen.

Figure 8

Correlation between FC and ARAT_post score of the BG. Increases in FC between the left BA5 and the right BA48 were positively correlated with ARAT_post score after training in the BG.

Figure 9

Correlation between FC and WMFT_post score of the BG. Increases in FC between the left BA5 and the right BA48 were positively correlated with WMFT_post score after training in the BG.