Enhancing Brain-Computer Interface Performance by Incorporating Brain-to-Brain Coupling.

Human cooperation relies on key features of social interaction in order to reach desirable outcomes. Similarly, human-robot interaction may benefit from integration with human-human interaction factors. In this paper, we aim to investigate brain-to-brain coupling during motor imagery (MI)-based brain-computer interface (BCI) training using eye-contact and hand-touch interaction. Twelve pairs of friends (experimental group) and 10 pairs of strangers (control group) were recruited for MI-based BCI tests concurrent with electroencephalography (EEG) hyperscanning. Event-related desynchronization (ERD) was estimated to measure cortical activation, and interbrain functional connectivity was assessed using multilevel statistical analysis. Furthermore, we compared BCI classification performance under different social interaction conditions. In the experimental group, greater ERD was found around the contralateral sensorimotor cortex under social interaction conditions compared with MI without any social interaction. Notably, EEG channels with decreased power were mainly distributed around the frontal, central, and occipital regions. A significant increase in interbrain coupling was also found under social interaction conditions. BCI decoding accuracies were significantly improved in the eye contact condition and eye and hand contact condition compared with the no-interaction condition. However, for the strangers' group, no positive effects were observed in comparisons of cortical activations between interaction and no-interaction conditions. These findings indicate that social interaction can improve the neural synchronization between familiar partners with enhanced brain activations and brain-to-brain coupling. This study may provide a novel method for enhancing MI-based BCI performance in conjunction with neural synchronization between users.

Brain-Computer Interface Priming for Cervical Transcutaneous Spinal Cord Stimulation Therapy: An Exploratory Case Study.

Loss of arm and hand function is one of the most devastating consequences of cervical spinal cord injury (SCI). Although some residual functional neurons often pass the site of injury, recovery after SCI is extremely limited. Recent efforts have aimed to augment traditional rehabilitation by combining exercise-based training with techniques such as transcutaneous spinal cord stimulation (tSCS), and movement priming. Such methods have been linked with elevated corticospinal excitability, and enhanced neuroplastic effects following activity-based therapy. In the present study, we investigated the potential for facilitating tSCS-based exercise-training with brain-computer interface (BCI) motor priming. An individual with chronic AIS A cervical SCI with both sensory and motor complete tetraplegia participated in a two-phase cross-over intervention whereby they engaged in 15 sessions of intensive tSCS-mediated hand training for 1 h, 3 times/week, followed by a two week washout period, and a further 15 sessions of tSCS training with bimanual BCI motor priming preceding each session. We found using the Graded Redefined Assessment for Strength, Sensibility, and Prehension that the participant's arm and hand function improved considerably across each phase of the study: from 96/232 points at baseline, to 117/232 after tSCS training alone, and to 131/232 points after BCI priming with tSCS training, reflecting improved strength, sensation, and gross and fine motor skills. Improved motor scores and heightened perception to sharp sensations improved the neurological level of injury from C4 to C5 following training and improvements were generally maintained four weeks after the final training session. Although functional improvements were similar regardless of the presence of BCI priming, there was a moderate improvement of bilateral strength only when priming preceded tSCS training, perhaps suggesting a benefit of motor priming for tSCS training.

Effect of Cervical Transcutaneous Spinal Cord Stimulation on Sensorimotor Cortical Activity during Upper-Limb Movements in Healthy Individuals.

Transcutaneous spinal cord stimulation (tSCS) can improve upper-limb motor function after spinal cord injury. A number of studies have attempted to deduce the corticospinal mechanisms which are modulated following tSCS, with many relying on transcranial magnetic stimulation to provide measures of corticospinal excitability. Other metrics, such as cortical oscillations, may provide an alternative and complementary perspective on the physiological effect of tSCS. Hence, the present study recorded EEG from 30 healthy volunteers to investigate if and how cortical oscillatory dynamics are altered by 10 min of continuous cervical tSCS. Participants performed repetitive upper-limb movements and resting-state tasks while tSCS was delivered to the posterior side of the neck as EEG was recorded simultaneously. The intensity of tSCS was tailored to each participant based on their maximum tolerance (mean: 50 ± 20 mA). A control session was conducted without tSCS. Changes to sensorimotor cortical activity during movement were quantified in terms of event-related (de)synchronisation (ERD/ERS). Our analysis revealed that, on a group level, there was no consistency in terms of the direction of ERD modulation during tSCS, nor was there a dose-effect between tSCS and ERD/ERS. Resting-state oscillatory power was compared before and after tSCS but no statistically significant difference was found in terms of alpha peak frequency or alpha power. However, participants who received the highest stimulation intensities had significantly weakened ERD/ERS (10% ERS) compared to when tSCS was not applied (25% ERD; p = 0.016), suggestive of cortical inhibition. Overall, our results demonstrated that a single 10 min session of tSCS delivered to the cervical region of the spine was not sufficient to induce consistent changes in sensorimotor cortical activity among the entire cohort. However, under high intensities there may be an inhibitory effect at the cortical level. Future work should investigate, with a larger sample size, the effect of session duration and tSCS intensity on cortical oscillations.

EEG Monitoring Is Feasible and Reliable during Simultaneous Transcutaneous Electrical Spinal Cord Stimulation.

Transcutaneous electrical spinal cord stimulation (tSCS) is a non-invasive neuromodulatory technique that has in recent years been linked to improved volitional limb control in spinal-cord injured individuals. Although the technique is growing in popularity there is still uncertainty regarding the neural mechanisms underpinning sensory and motor recovery. Brain monitoring techniques such as electroencephalography (EEG) may provide further insights to the changes in coritcospinal excitability that have already been demonstrated using other techniques. It is unknown, however, whether intelligible EEG can be extracted while tSCS is being applied, owing to substantial high-amplitude artifacts associated with stimulation-based therapies. Here, for the first time, we characterise the artifacts that manifest in EEG when recorded simultaneously with tSCS. We recorded multi-channel EEG from 21 healthy volunteers as they took part in a resting state and movement task across two sessions: One with tSCS delivered to the cervical region of the neck, and one without tSCS. An offline analysis in the time and frequency domain showed that tSCS manifested as narrow, high-amplitude peaks with a spectral density contained at the stimulation frequency. We quantified the altered signals with descriptive statistics-kurtosis, root-mean-square, complexity, and zero crossings-and applied artifact-suppression techniques-superposition of moving averages, adaptive, median, and notch filtering-to explore whether the effects of tSCS could be suppressed. We found that the superposition of moving averages filter was the most successful technique at returning contaminated EEG to levels statistically similar to that of normal EEG. In the frequency domain, however, notch filtering was more effective at reducing the spectral power contribution of stimulation from frontal and central electrodes. An adaptive filter was more appropriate for channels closer to the stimulation site. Lastly, we found that tSCS posed no detriment the binary classification of upper-limb movements from sensorimotor rhythms, and that adaptive filtering resulted in poorer classification performance. Overall, we showed that, depending on the analysis, EEG monitoring during transcutaneous electrical spinal cord stimulation is feasible. This study supports future investigations using EEG to study the activity of the sensorimotor cortex during tSCS, and potentially paves the way to brain-computer interfaces operating in the presence of spinal stimulation.

EEG Correlates of Self-Managed Neurofeedback Treatment of Central Neuropathic Pain in Chronic Spinal Cord Injury.

BACKGROUND: Neurofeedback (NFB) is a neuromodulatory technique that enables voluntary modulation of brain activity in order to treat neurological condition, such as central neuropathic pain (CNP). A distinctive feature of this technique is that it actively involves participants in the therapy. In this feasibility study, we present results of participant self-managed NFB treatment of CNP. METHODS: Fifteen chronic spinal cord injured (SCI) participants (13M, 2F), with chronic CNP equal or greater than 4 on the Visual Numeric Scale, took part in the study. After initial training in hospital (up to 4 sessions), they practiced NF at home, on average 2-3 times a week, over a period of several weeks (min 4, max 20). The NFB protocol consisted of upregulating the alpha (9-12 Hz) and downregulating the theta (4-8 Hz) and the higher beta band (20-30 Hz) power from electrode location C4, for 30 min. The output measures were pain before and after NFB, EEG before and during NFB and pain questionnaires. We analyzed EEG results and show NFB strategies based on the Power Spectrum Density of each single participant. RESULTS: Twelve participants achieved statistically significant reduction in pain and in eight participants this reduction was clinically significant (larger than 30%). The most successfully regulated frequency band during NFB was alpha. However, most participants upregulated their individual alpha band, that had an average dominant frequency at αp = 7.6 ± 0.8 Hz (median 8 Hz) that is lower than the average of the general population, which is around 10 Hz. Ten out of fifteen participants significantly upregulated their individual alpha power (αp ± 2 Hz) as compared to 4 participants who upregulated the power in the fixed alpha band (8-12 Hz). Eight out of the twelve participants who achieved a significant reduction of pain, significantly upregulated their individual alpha band power. There was a significantly larger increase in alpha power (p < 0.0001) and decrease of theta power (p < 0.04) in participant specific rather than in fixed frequency bands. CONCLUSION: Neurofeedback is a neuromodulatory technique that gives participants control over their pain and can be self-administered at home. Regulation of individual frequency band was related to a significant reduction in pain.