Ipsilesional Mu Rhythm Desynchronization and Changes in Motor Behavior Following Post Stroke BCI Intervention for Motor Rehabilitation

Abstract

Loss of motor function is a common deficit following stroke insult and often manifests as persistent upper extremity (UE) disability which can affect a survivor's ability to participate in activities of daily living. Recent research suggests the use of brain-computer interface (BCI) devices might improve UE function in stroke survivors at various times since stroke. This randomized crossover-controlled trial examines whether intervention with this BCI device design attenuates the effects of hemiparesis, encourages reorganization of motor related brain signals (EEG measured sensorimotor rhythm desynchronization), and improves movement, as measured by the Action Research Arm Test (ARAT). A sample of 21 stroke survivors, presenting with varied times since stroke and levels of UE impairment, received a maximum of 18-30 h of intervention with a novel electroencephalogram-based BCI-driven functional electrical stimulator (EEG-BCI-FES) device. Driven by spectral power recordings from contralateral EEG electrodes during cued attempted grasping of the hand, the user's input to the EEG-BCI-FES device modulates horizontal movement of a virtual cursor and also facilitates concurrent stimulation of the impaired UE. Outcome measures of function and capacity were assessed at baseline, mid-therapy, and at completion of therapy while EEG was recorded only during intervention sessions. A significant increase in r-squared values [reflecting Mu rhythm (8-12 Hz) desynchronization as the result of attempted movements of the impaired hand] presented post-therapy compared to baseline. These findings suggest that intervention corresponds with greater desynchronization of Mu rhythm in the ipsilesional hemisphere during attempted movements of the impaired hand and this change is related to changes in behavior as a result of the intervention. BCI intervention may be an effective way of addressing the recovery of a stroke impaired UE and studying neuromechanical coupling with motor outputs. Clinical Trial Registration: ClinicalTrials.gov, identifier NCT02098265.

Keywords: brain–computer interface;; hemiparesis; r-squared; coherence; chronic; acute; neuroplasticity; homunculus.

FIGURE 1

Study design. The time-points at which neuroimaging data were collected are represented by, T1, control baseline; T2, control middle; T3, control completion; T4, intervention baseline; T5, mid-intervention; T6, completion of intervention; T7, 1-month post-intervention. While the crossover control group (DTG) completed visits T1 through T7, the immediate therapy (ITG) group completed only visits T4 through T7. EEG-BCI-FES intervention is only administered during the BCI Therapy Phase (green), from baseline (T4) to completion (T6), and EEG recordings are neither acquired between T1 and T4, nor between T6 and T7 during which only MRI and behavioral testing batteries are administered. EEG data were only collected during the intervention phase.

FIGURE 2

BCI intervention block design. (1) Pre-screening (two actual movement trials, two imagined movement trials). (2) Cursor task (≥10 trials with visual-only feedback). (3) Cursor task with adjuvant stimuli (≥10 trials with adjuvant stimuli). (4) Post-screening (two imagined movement trials, two actual movement trials).

FIGURE 3

BCI cap array. Electrode array and cap arrangement for all n = 21 participants. Control signals generated at C3 and C4 electrodes for right and left hand movement trials, respectively. Ear clip always placed on the right ear.

FIGURE 4

Topographical plots (topoplots) of grand averages for Mu rhythm (8–12 Hz) signed r-squared values at group level (n = 21). The bar plot shows the group means for the Mu rhythm signed r-squared values from the impaired hand attempted movement trials (vs. rest) at ipsilesional electrode site. Asterisk denotes statistical significance from a one-tailed paired t-test (p < 0.05). Error bars denote standard error of the mean. The majority of participants were left hand impaired. Prescreening, open-looped training (PRE) and open-looped post screening BCI training (POST) runs (color bar: [–0.2 = blue – 0.2 = red]). The majority of participants had a right lateralized lesion.

FIGURE 5

Topoplots of grand averages for signed r-squared values at group level (n = 21) for attempted movements. In the top two rows of topoplots, a larger negative value (blue) denotes stronger desynchronization (rest vs. left or right hand actual movement); in the bottom row of topoplots a larger positive value (red) denotes desynchronization (left vs. right hand actual movements). The mentioned distinction reflects the way in which the signed r-squared values were calculated in a rest vs. left/or right comparison, and in a left vs. right comparison. Prescreening, open-looped training (PRE) and open-looped post screening BCI training (POST) runs (color bar: [–0.2 = blue – 0.2 = red]). The majority of participants had a right lateralized lesion.

FIGURE 6

Topoplots of grand averaged coherence values at group level (n = 21) for Mu (8–12 Hz) and Beta (18–26 Hz) bands during attempted movement trials. Prescreening, open-looped training (PRE) and open-looped post screening BCI training (POST) runs (color bar: [0 = blue – 0.5 = red]). The majority of participants had a right lateralized lesion.

FIGURE 7

Topoplots of grand averages for signed r-squared values at group level (n = 21) for imaginary movements. Prescreening, open-looped training (PRE) and open-looped post screening BCI training (POST) runs (color bar: [0 = blue – 0.5 = red]). The majority of participants had a right lateralized lesion.

FIGURE 8

Topoplots of grand averaged coherence values at group level (n = 21) for Mu (8–12 Hz) and Beta (18–26 Hz) bands during imaginary movement trials. Prescreening, open-looped training (PRE) and open-looped post screening BCI training (POST) runs (color bar: [0 = blue – 0.5 = red]). The majority of participants had a right lateralized lesion.

FIGURE 9

Association between the change in r-squared values (Beta band, 18–26 Hz) as the result of BCI training with the total number of cursor trial (i.e., intervention) runs [r(20) = 0.393; p = 0.043].

FIGURE 10

Association between the change in r-squared values (Mu rhythm, 8–12 Hz) as the result of BCI training with the change in ARAT scores (obtained post-intervention in comparison to baseline) [ρ(20) = 0.30; p = 0.098].