Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface

Abstract

Mrachacz-Kersting N, Jiang N, Stevenson AJ, Niazi IK, Kostic V, Pavlovic A, Radovanovic S, Djuric-Jovicic M, Agosta F, Dremstrup K, Farina D. Efficient neuroplasticity induction in chronic stroke patients by an associative brain-computer interface. J Neurophysiol 115: 1410 -1421, 2016. First published December 30, 2015 doi:10.1152/jn.00918.2015 have the potential to improve functionality in chronic stoke patients when applied over a large number of sessions. Here we evaluated the effect and the underlying mechanisms of three BCI training sessions in a double-blind sham-controlled design. The applied BCI is based on Hebbian principles of associativity that hypothesize that neural assemblies activated in a correlated manner will strengthen synaptic connections. Twenty-two chronic stroke patients were divided into two training groups. Movement-related cortical potentials (MRCPs) were detected by electroencephalography during repetitions of foot dorsiflexion. Detection triggered a single electrical stimulation of the common peroneal nerve timed so that the resulting afferent volley arrived at the peak negative phase of the MRCP (BCI associative group) or randomly (BCI nonassociative group). Fugl-Meyer motor assessment (FM), 10-m walking speed, foot and hand tapping frequency, diffusion tensor imaging (DTI) data, and the excitability of the corticospinal tract to the target muscle [tibialis anterior (TA)] were quantified. The TA motor evoked potential (MEP) increased significantly after the BCI associative intervention, but not for the BCI nonassociative group. FM scores (0.8 Ϯ 0.46 point difference, P ϭ 0.01), foot (but not finger) tapping frequency, and 10-m walking speed improved significantly for the BCI associative group, indicating clinically relevant improvements. Corticospinal tract integrity on DTI did not correlate with clinical or physiological changes. For the BCI as applied here, the precise coupling between the brain command and the afferent signal was imperative for the behavioral, clinical, and neurophysiological changes reported. This association may become the driving principle for the design of BCI rehabilitation in the future. Indeed, no available BCIs can match this degree of functional improvement with such a short intervention.

Brain‐computer interfaces for post‐stroke motor rehabilitation: a meta‐analysis

“…showed improved ipsilesional connectivity in the mu and beta bands after BCI‐NMES training compared to a group undergoing placebo‐BCI training. Other studies have reported shifts in hemispheric EEG activity41 and increase in ipsilesional movement‐related cortical potentials as well as motor‐evoked potentials 56. In addition, some of these neurophysiological measures correlated with behavioral improvements: (1) EEG‐based Brain Symmetry index could predict the functional motor outcomes in Ang et al.…”

“…We also identified three studies that targeted lower limb: (1) Mrachacz‐Kersting et al 56. reported improvements in FMA for lower extremity score (mean difference of 0.8 ± 0.46) in chronic stroke patients ( N  = 22), where they estimated reaction time from offline EEG, which was then used for delivering peroneal nerve stimulation during interventional trials (i.e., online trials), but not in the sham feedback group.…”

Influence of attention alternation on movement-related cortical potentials in healthy individuals and stroke patients

“…The MRCP is a slow cortical potential that has been associated with voluntarily executed, self-paced or imagined movements (Hallett, 1994). By pairing the intent of the participant with the artificial production of the imagined or intended movement, we have shown significant plastic changes within the motor cortex of both healthy participants and patients (Scheel et al, 2015;Mrachacz-Kersting et al, 2015). Patients also significantly increased their 10 m walking speed and foot tapping frequency.…”

Rehabilitation of hand in subacute tetraplegic patients based on brain computer interface and functional electrical stimulation: a randomised pilot study

“…In a study by Mrachacz-Kersting et al (2016) only patients receiving a single pulse stimulus precisely matched with the maximum negativity of MRCP improved their speed of walking. Interestingly, although patients practiced isolated ballistic foot dorsiflexion it translated to the improvement of walking.…”