Brain–computer interface-based action observation combined with peripheral electrical stimulation enhances corticospinal excitability in healthy subjects and stroke patients

Abstract

Objective: Action observation (AO) combined with brain computer interface (BCI) technology enhances the cortical activation. Peripheral electrical stimulation (PES) is known to increase the corticospinal excitability, thereby activating brain plasticity. To maximize motor recovery, we assessed the effects of BCI-AO combined with PES on corticospinal plasticity. Approach: Seventeen patients with chronic hemiplegic stroke and 17 healthy subjects were recruited. The participants watched a video of repetitive grasping actions with four different tasks for 15 mins: A) AO alone; B) AO + PES; C) BCI-AO + continuous PES; D) BCI-AO + triggered PES. PES was applied at the ulnar nerve of the wrist. The tasks were performed in a random order at least 3 days apart. We assessed the latency and amplitude of the motor evoked potentials (MEPs). We examined changes in MEP parameters pre-and post-exercise across the four tasks in the FDI muscle of the dominant hand (healthy subjects) and affected hand (stroke patients). Main results: The decrease in MEP latency and increase in MEP amplitude after the four tasks were significant in both groups. The increase in MEP amplitude was sustained for 20 mins after tasks B, C, and D in both groups. The increase in MEP amplitude was significant between tasks A vs B, B vs C, and C vs D. The estimated mean difference in MEP amplitude post-exercise was highest for A and D in both groups. Significance: The results indicate that BCI-AO combined with PES is superior to AO alone or AO + PES for facilitating corticospinal plasticity in both healthy subjects and stroke patients. Furthermore, this study supports the idea that synchronized activation of cortical and peripheral networks can enhance neuroplasticity after stroke. We suggest that the BCI-AO paradigm and PES could provide a novel neurorehabilitation strategy for stroke patients.

Effectiveness of motor and prefrontal cortical areas for brain-controlled functional electrical stimulation neuromodulation

“…Our M1 intervention findings are in agreement with the proposed mechanism that BCI-FES usage involves Hebbian-like learning [9,[16][17][18]. In short, the repeated presynaptic cortical activation detected by the BCI system, which is closely followed by postsynaptic sensory nerve activation and movement-related reafference elicited using FES, could strengthen corticospinal projections after the intervention, as previously proposed [3,9,16,18]. The M1 area has direct corticospinal projections to the spinal motoneurons [14].…”

“…Non-invasive brain-computer interface (BCI)controlled functional electrical stimulation (FES) has been postulated to have the potential to contribute to the recovery of upper limb motor function after stroke [1][2][3][4][5][6] and incomplete spinal cord injury (SCI) [7,8]. The motor facilitation after the use of BCI-controlled FES has been reported to be associated with corticospinal [3] and cortical [1,2,5] excitability.…”

“…Non-invasive brain-computer interface (BCI)controlled functional electrical stimulation (FES) has been postulated to have the potential to contribute to the recovery of upper limb motor function after stroke [1][2][3][4][5][6] and incomplete spinal cord injury (SCI) [7,8]. The motor facilitation after the use of BCI-controlled FES has been reported to be associated with corticospinal [3] and cortical [1,2,5] excitability. BCI-FES could induce such facilitation by applying activity-dependent stimulation during therapeutic interventions, which are typically delivered over multiple sessions and longerduration ranging between 2 and 14 weeks [1,2,[4][5][6][7][8].…”

“…BCI-FES could induce such facilitation by applying activity-dependent stimulation during therapeutic interventions, which are typically delivered over multiple sessions and longerduration ranging between 2 and 14 weeks [1,2,[4][5][6][7][8]. Interestingly, studies with non-disabled participants also suggested that BCI-controlled FES can induce rapid corticospinal excitability facilitation after a short-duration session [3,9,10].…”

Attentional state-synchronous peripheral electrical stimulation during action observation induced distinct modulation of corticospinal plasticity after stroke

“…A previous study introduced the concept of attentional state-dependent PES during the AO paradigm using the BCI-SSVEPs protocol (Kim et al, 2022 ). The results indicated that the attentional state-dependent PES task was superior to AO alone or to a simple combination of AO and PES in facilitating corticospinal plasticity in both patients with stroke and in healthy individuals (Kim et al, 2022 ). Moreover, this paradigm is effective in enhancing sensorimotor cortical activation in the affected hemispheres of stroke patients (Lim et al, 2023 ).…”