Using ipsilateral motor signals in the unaffected cerebral hemisphere as a signal platform for brain–computer interfaces in hemiplegic stroke survivors

Abstract

Objective Brain computer interface (BCI) systems have emerged as a method to restore function and enhance communication in motor impaired patients. To date, this has been primarily applied to patients who have a compromised motor outflow due to spinal cord dysfunction, but an intact and functioning cerebral cortex. The cortical physiology associated with movement of the contralateral limb has typically been the signal substrate that has been used as a control signal. While this is an ideal control platform in patients with an intact motor cortex, these signals are lost after a hemispheric stroke. Thus, a different control signal is needed that could provide control capability for a patient with a hemiparetic limb. Previous studies have shown that there is a distinct cortical physiology associated with ipsilateral, or same sided, limb movements. Thus far, it was unknown whether stroke survivors could intentionally and effectively modulate this ipsilateral motor activity from their unaffected hemisphere. Therefore, this study seeks to evaluate whether stroke survivors could effectively utilize ipsilateral motor activity from their unaffected hemisphere to achieve this BCI control. Approach To investigate this possibility, electroencephalographic (EEG) signals were recorded from four chronic hemispheric stroke patients as they performed (or attempted to perform) real and imagined hand tasks using either their affected or unaffected hand. Following performance of the screening task, the ability of patients to utilize a BCI system was investigated during on-line control of a 1-dimensional control task. Main Results Significant ipsilateral motor signals (associated with movement intentions of the affected hand) in the unaffected hemisphere, which were found to be distinct from rest and contralateral signals, were identified and subsequently used for a simple online BCI control task. We demonstrate here for the first time that EEG signals from the unaffected hemisphere, associated with overt and imagined movements of the affected hand, can enable stroke survivors to control a one-dimensional computer cursor rapidly and accurately. This ipsilateral motor activity enabled users to achieve final target accuracies between 68 and 91% within 15 minutes. Significance These findings suggest that ipsilateral motor activity from the unaffected hemisphere in stroke survivors could provide a physiological substrate for BCI operation that can be further developed as a long-term assistive device or potentially provide a novel tool for rehabilitation.

Robust Neuroprosthetic Control from the Stroke Perilesional Cortex

“…In other words, whereas the PLC is capable of expressing plasticity, the lack of a substrate to transmit the information ultimately prevents motor recovery. Moreover, our finding of robust direct neural control of the PLC may have implications for emerging therapeutics; for example, cell-based therapies aim to augment the plasticity and the recovery potential of cortical areas after stroke (Bliss et al, 2007).…”

“…Taskdependent volitional modulation of the activity of selected neurons is also closely tied to the concept of BMIs (Fetz, 1969;Koralek et al, 2010;. Together, this body of work has also indicated that neural plasticity likely plays an important role in achieving stable neuroprosthetic control (Taylor et al, 2002;Jarosiewicz et al, 2008;Moritz et al, 2008;Koralek et al, 2010;Arduin et al, 2013;Gulati et al, 2014). Importantly, this research into the development of intracortical BMIs has primarily focused on subjects with intact cortical structures.…”

“…In contrast, the development of BMIs specifically compatible with stroke (Langhorne et al, 2011;Norrving and Kissela, 2013) or other forms of direct cortical injury requires a greater understanding of the neurophysiology of the injured neural network (Nudo et al, 1996;Ward, 2004;Dancause, 2006;Cramer, 2008;Murphy and Corbett, 2009). Although both the perilesional cortex (PLC) surrounding the injury (Daly and Wolpaw, 2008;Guggenmos et al, 2013) and motor areas in the unaffected hemisphere are possible targets of neural interfaces after stroke, more attention has been placed on the unaffected contralateral hemisphere (Bundy et al, 2012).…”

“…However, the PLC is an important site of reorganization after stroke (Nudo and Milliken, 1996; Brown et al, 2010); moreover, task-specific rehabilitation is also known to have synergistic effects on perilesional cortical plasticity (Nudo et al, 1996;Bier-naskie and Corbett, 2001;. It remains unknown whether the impaired local structural and functional connectivity present after stroke (Nudo et al, 1996;Ward, 2004;Dancause, 2006;Cramer, 2008;Murphy and Corbett, 2009;Guggenmos et al, 2013) can support neuroprosthetic control. By adapting chronic electrophysiological recordings to a rodent stroke model, we investigated the electrophysiological characteristics of the injured PLC and whether its spiking activity can be modulated volitionally to control an artificial actuator.…”

Brain–machine interfaces in neurorehabilitation of stroke

“…Advances in the field of telerehabilitation allowing for monitoring physiological parameters and treatment course may facilitate application of BMIs in home-based rehabilitation programs. In cases in which ipsilesional BMI training is not feasible due to the absence of brain signals to be trained and where the possibility to augment such signal by brain stimulation or other means is unavailable, training of contralesional, ipsilateral brain activity might be a possible alternative (Bundy et al, 2012;Carmena, 2013).…”