Contralesional Brain–Computer Interface Control of a Powered Exoskeleton for Motor Recovery in Chronic Stroke Survivors

Bundy, David T.; Souders, Lauren; Baranyai, Kelly; Leonard, Laura D.; Schalk, Gerwin; Coker, Robert; Moran, Daniel W.; Huskey, Thy; Leuthardt, Eric C.

doi:10.1161/strokeaha.116.016304

Cited by 179 publications

(173 citation statements)

References 33 publications

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“…Known pathophysiology in stroke‐lesioned brains is a reduction of the modulation of the sensorimotor beta rhythm in chronic stroke patients compared to healthy subjects . Also, current experimental approaches of noninvasive brain‐computer interfaces for upper limb rehabilitation mostly exploit the sensorimotor alpha and beta rhythms . Thus, we tested whether the described diminishment of movement‐related LFOs poststroke and re‐emergence are specific for LFOs, or whether similar patterns occur in typically studied sensorimotor rhythms in the alpha and beta range (Fig 5).…”

Section: Resultsmentioning

confidence: 99%

“…23,29,30 Also, current experimental approaches of noninvasive brain-computer interfaces for upper limb rehabilitation mostly exploit the sensorimotor alpha and beta rhythms. 31,32 Thus, we tested whether the described diminishment of movement-related LFOs poststroke and reemergence are specific for LFOs, or whether similar patterns occur in typically studied sensorimotor rhythms in the alpha and beta range ( Fig 5). We first analyzed the temporal pattern of alpha (8-13Hz) and beta (15-22Hz) modulation around grip onset in the healthy controls.…”

Section: Specificity Of Power Re-emergence To Lfosmentioning

confidence: 99%

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Low‐Frequency Brain Oscillations Track Motor Recovery in Human Stroke

Bönstrup

Krawinkel

Schulz

et al. 2019

Annals of Neurology

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Objective The majority of patients with stroke survive the acute episode and live with enduring disability. Effective therapies to support recovery of motor function after stroke are yet to be developed. Key to this development is the identification of neurophysiologic signals that mark recovery and are suitable and susceptible to interventional therapies. Movement preparatory low‐frequency oscillations (LFOs) play a key role in cortical control of movement. Recent animal data point to a mechanistic role of motor cortical LFOs in stroke motor deficits and demonstrate neuromodulation intervention with therapeutic benefit. Their relevance in human stroke pathophysiology is unknown. Methods We studied the relationship between movement‐preparatory LFOs during the performance of a visuomotor grip task and motor function in a longitudinal (<5 days, 1 and 3 months) cohort study of 33 patients with motor stroke and in 19 healthy volunteers. Results Acute stroke–lesioned brains fail to generate the LFO signal. Whereas in healthy humans, a transient occurrence of LFOs preceded movement onset at predominantly contralateral frontoparietal motor regions, recordings in patients revealed that movement‐preparatory LFOs were substantially diminished to a level of 38% after acute stroke. LFOs progressively increased at 1 and 3 months. This re‐emergence closely tracked the recovery of motor function across several movement qualities including grip strength, fine motor skills, and synergies and was frequency band specific. Interpretation Our results provide the first human evidence for a link between movement‐preparatory LFOs and functional recovery after stroke, promoting their relevance for movement control. These results suggest that it may be interesting to explore targeted, LFOs‐restorative brain stimulation therapy in human stroke patients. ANN NEUROL 2019;86:853–865

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Section: Resultsmentioning

confidence: 99%

Section: Specificity Of Power Re-emergence To Lfosmentioning

confidence: 99%

Low‐Frequency Brain Oscillations Track Motor Recovery in Human Stroke

Bönstrup

Krawinkel

Schulz

et al. 2019

Annals of Neurology

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“…Specifically, most BCI‐based motor rehabilitation systems have traditionally encompassed neural activity decoders of ipsilesional sensorimotor activity (sensorimotor rhythm, SMR, 9–15 Hz). Interestingly, a few recent studies suggest promoting contralesional hemispheric activity in moderate‐to‐severe chronic post‐stroke patients, with an assumption that it may be harder to measure stable SMR from the ipsilesional sensorimotor areas in this group of patients 28. Depending on the study protocol, BCI‐mediated training may promote activity in the ipsilesional or contralesional hemisphere 29…”

Section: Introductionmentioning

confidence: 99%

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

Cervera

Soekadar

Ushiba

et al. 2018

Ann Clin Transl Neurol

366

267

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Brain‐computer interfaces (BCIs) can provide sensory feedback of ongoing brain oscillations, enabling stroke survivors to modulate their sensorimotor rhythms purposefully. A number of recent clinical studies indicate that repeated use of such BCIs might trigger neurological recovery and hence improvement in motor function. Here, we provide a first meta‐analysis evaluating the clinical effectiveness of BCI‐based post‐stroke motor rehabilitation. Trials were identified using MEDLINE, CENTRAL, PEDro and by inspection of references in several review articles. We selected randomized controlled trials that used BCIs for post‐stroke motor rehabilitation and provided motor impairment scores before and after the intervention. A random‐effects inverse variance method was used to calculate the summary effect size. We initially identified 524 articles and, after removing duplicates, we screened titles and abstracts of 473 articles. We found 26 articles corresponding to BCI clinical trials, of these, there were nine studies that involved a total of 235 post‐stroke survivors that fulfilled the inclusion criterion (randomized controlled trials that examined motor performance as an outcome measure) for the meta‐analysis. Motor improvements, mostly quantified by the upper limb Fugl‐Meyer Assessment (FMA‐UE), exceeded the minimal clinically important difference (MCID=5.25) in six BCI studies, while such improvement was reached only in three control groups. Overall, the BCI training was associated with a standardized mean difference of 0.79 (95% CI: 0.37 to 1.20) in FMA‐UE compared to control conditions, which is in the range of medium to large summary effect size. In addition, several studies indicated BCI‐induced functional and structural neuroplasticity at a subclinical level. This suggests that BCI technology could be an effective intervention for post‐stroke upper limb rehabilitation. However, more studies with larger sample size are required to increase the reliability of these results.

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“…The main reasons for excluding the other 282 (by title and/or abstract) were no randomized controlled trials or nonrandomized trails, BCI was not used as an intervention or related to upper limb rehabilitation or had no upper limb functional assessment, population differed from the predefined criteria, articles regarding intervention on animals or focused on methodology, virtual reality environments or neuroprostheses without a brain interface, and mirror therapy. From the 26 articles remaining, 17 were excluded after reading the full document (Ang et al, ; Bundy et al, ; Cincotti et al, ; Curado et al, ; Kasashima‐Shindo et al, ; Kawakami et al, ; Liu et al, ; Mrachacz‐Kersting et al, ; Ono et al, ; Pichiorri et al, ; Rayegani et al, ; Ushiba, Morishita, & Maeda, ; Varkuti et al, ; Wang, Liu, Zhang, Li, & Zhang, ; Wu et al, ; Young, Nigogosyan, Remsik, et al, ; Young et al, ; see Figure ). No new articles were retrieved by using reference and author tracking.…”

Section: Resultsmentioning

confidence: 99%

Brain‐machine interface of upper limb recovery in stroke patients rehabilitation: A systematic review

Carvalho

Dias

Cerqueira

2019

Physiotherapy Res Intl

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Background Technologies such as brain‐computer interfaces are able to guide mental practice, in particular motor imagery performance, to promote recovery in stroke patients, as a combined approach to conventional therapy. Objective The aim of this systematic review was to provide a status report regarding advances in brain‐computer interface, focusing in particular in upper limb motor recovery. Methods The databases PubMed, Scopus, and PEDro were systematically searched for articles published between January 2010 and December 2017. The selected studies were randomized controlled trials involving brain‐computer interface interventions in stroke patients, with upper limb assessment as primary outcome measures. Reviewers independently extracted data and assessed the methodological quality of the trials, using the PEDro methodologic rating scale. Results From 309 titles, we included nine studies with high quality (PEDro ≥ 6). We found that the most common interface used was non‐invasive electroencephalography, and the main neurofeedback, in stroke rehabilitation, was usually visual abstract or a combination with the control of an orthosis/robotic limb. Moreover, the Fugl–Meyer Assessment Scale was a major outcome measure in eight out of nine studies. In addition, the benefits of functional electric stimulation associated to an interface were found in three studies. Conclusions Neurofeedback training with brain‐computer interface systems seem to promote clinical and neurophysiologic changes in stroke patients, in particular those with long‐term efficacy.

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Contralesional Brain–Computer Interface Control of a Powered Exoskeleton for Motor Recovery in Chronic Stroke Survivors

Abstract: Supplemental Digital Content is available in the text.

Cited by 179 publications

References 33 publications

Low‐Frequency Brain Oscillations Track Motor Recovery in Human Stroke

Low‐Frequency Brain Oscillations Track Motor Recovery in Human Stroke

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

Brain‐machine interface of upper limb recovery in stroke patients rehabilitation: A systematic review

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