Controlling pre-movement sensorimotor rhythm can improve finger extension after stroke

Abstract

Objective: Brain-computer interface (BCI) technology is attracting increasing interest as a tool for enhancing recovery of motor function after stroke, yet the optimal way to apply this technology is unknown. Here, we studied the immediate and therapeutic effects of BCI-based training to control pre-movement sensorimotor rhythm (SMR) amplitude on robot-assisted finger extension in people with stroke.

Approach: Eight people with moderate to severe hand impairment due to chronic stroke completed a four-week three-phase protocol during which they practiced finger extension with assistance from the FINGER robotic exoskeleton. In Phase 1, we identified spatiospectral SMR features for each person that correlated with the intent to extend the index and/or middle finger(s). In Phase 2, the participants learned to increase or decrease SMR features given visual feedback, without movement. In Phase 3, the participants were cued to increase or decrease their SMR features, and when successful, were then cued to immediately attempt to extend the finger(s) with robot assistance.

Main results: Of the four participants that achieved SMR control in Phase 2, three initiated finger extensions with a reduced reaction time after decreasing (versus increasing) pre-movement SMR amplitude during Phase 3. Two also extended at least one of their fingers more forcefully after decreasing pre-movement SMR amplitude. Hand function, measured by the box and block test (BBT), improved by 7.3 ± 7.5 blocks versus 3.5 ± 3.1 blocks in those with and without SMR control, respectively. Higher BBT scores at baseline correlated with a larger change in BBT score.

Significance: These results suggest that learning to control person-specific pre-movement SMR features associated with finger extension can improve finger extension ability after stroke for some individuals. These results merit further investigation in a rehabilitation context.

Figures

Figure 1:

Timeline of study. Each dot represents a day with one session of training. Each group of three dots represents one week of training (4 weeks total). Red dots are robot-assisted movement sessions; blue dots are BCI-based SMR/visual feedback-only sessions; blue/red dots are sessions in which SMR control triggered robot-assisted movement. Phases 1 and 3 had three sessions each, while phase 2 had six sessions. Movement (finger extension) analyses are indicated (m). Clinical assessments (c) of upper-extremity movement ability (Box & Block) were conducted at the beginning and end of phases 1 and 3.

Figure 2:

Trial progressions are shown for phases 1–3. BCI control components are in boxes outlined in blue; robot-assisted movements are in boxes outlined in red. Phase 1: Participants are cued to attempt extension of the index finger, middle finger, or both. Shown here are the visual cues for an index finger trial. (a); an index movement preparation warning cue (yellow dot); (b): the imperative “Go” cue for an index finger movement (green dot); (c): the participant’s correct response (index finger extension) elicits robot assistance for the remainder of the movement and visual feedback occurs (green dot grows with finger position); (d): the dot turns white indicating a properly executed movement. Phase 2: The participant attempts to increase SMR amplitude for targets of one color (yellow or blue) and decrease SMR amplitude for targets of the other color. (e): a yellow square appears, prompting this participant to increase SMR amplitude (a blue square would prompt SMR decrease in this participant); (f) the square brightens as SMR amplitude approaches the criterion; (g) satisfying the criterion for 1 s produces a green square indicating success; (h) the screen goes blank for 2.5 s. Phase 3: (i): as in Phase 2, this participant modulates SMR amplitude; (j) as SMR amplitude approaches and satisfies the criterion value, the square brightens; (k) when the SMR criterion is satisfied for the required 1 s, a movement stimulus appears; (l) the green circle grows with finger extension; (m) if the movement is properly executed, the green circle turns white; the screen is blank for 2.5 s and the robot returns the participant’s finger to the starting position.

Figure 3:

BCI hit rates across the Phase-2 sessions for each participant. Chance accuracy is 50% (dotted line). Four participants (a, b, c, d, in black) learned to control SMR amplitude. Two participants (e and f, in blue) exhibited broad spatiospectral patterns (see Fig. 4) indicative of control by head/neck muscle activity rather than actual SMR amplitude modulation. Two participants (g and h) did not gain control.

Figure 4:

Topographies and spectra of the correlation (R-value) between the SMR feature amplitude and the target condition, SMR down-regulation (red) vs. SMR up-regulation (black). Data from the last phase2 session are shown for each participant, a through h. Topographies and power spectra were generated using a bipolar reference to channel Cz; the specific channel used to generate the spectra for each participant is indicated. Asterisks denote the stroke-affected hemisphere. Participants a, b, c, and d exhibited narrow-band BCI control (arrows). Participants e and f showed broad-band control indicative of artifactual (i.e., probably head/neck muscle) activity. Participants g and h did not show significant control, although participant h did produce a narrow-band differential signal.

Figure 5:

Participants a, b, c, and d exhibited narrow-band BCI control above chance level. Participants e and f exhibited broad-band artifactual (i.e., head/neck muscle-based) control. Participants g and h did not achieve control. Thus, further analyses of the effects of BCI training on motor performance excluded participants e-h.

Figure 6:

All phase-3 index finger movements from participants a, b, c, and d. Index finger position (left) and normalized MCP torque (right) are plotted vs. time where t=0 corresponds to the movement cue. Yellow traces represent responses to stimuli that increased SMR and blue traces represent responses to stimuli that decreased SMR. Movement latencies were significantly shorter for a, c, and d when they decreased pre-movement SMR amplitude vs. when they increased it. MCP torques were significantly higher for participants a and c when they decreased pre-movement SMR amplitude. Note that the torque values were normalized by the maximum torque generated by each subject in all three different finger movement conditions, although only the index finger movements are shown here.

Figure 7:

SMR amplitudes and corresponding Phase-3 performance for each movement (i.e. index finger, middle finger, both fingers) from participants a, b, c, and d for SMR increase (yellow) and SMR decrease (blue) trials. Left: Average pre-movement SMR amplitude; Middle: Average latencies to movement onset; Right: Average peak MCP torques. Stars indicate significance (p

Figure 8:

Box & Block scores for each participant taken at baseline and the beginnings and ends of phase 1 (sessions 1 and 3) and phase 3 (sessions 10 and 12). Participants who gained SMR control are shown in black. Participants e and f, who used broadband (i.e., muscle-based) activity to control the BCI, are shown in blue. Participants g and h, who did not gain any control, are shown in red.

Figure 9:

Left: Box & Block Test (BBT) score, measured at baseline, was correlated with a change in BBT score after therapy, measured as the change in score at the end of therapy compared to the average of the baseline and session 1 score. Higher BBT scores at baseline were correlated with larger gains in BBT score after therapy for all participants. Right: Relationship between BBT measured at baseline and the change in latency for finger movements after therapy (session 12 vs. session 1). Positive change in latency values indicates slower response times and negative values indicate faster response times. Higher BBT scores at baseline were correlated with larger reductions in latency after therapy for participants with BCIcontrol (a-d). Participants e and f, who used artifactual (i.e., head/neck muscle-based) activity to control the BCI, are shown in blue. Participants g and h, who did not gain control of the BCI, are shown in red.