Brain-Machine Interface in Chronic Stroke: Randomized Trial Long-Term Follow-up.

BACKGROUND: Brain-machine interfaces (BMIs) have been recently proposed as a new tool to induce functional recovery in stroke patients. OBJECTIVE: Here we evaluated long-term effects of BMI training and physiotherapy in motor function of severely paralyzed chronic stroke patients 6 months after intervention. METHODS: A total of 30 chronic stroke patients with severe hand paresis from our previous study were invited, and 28 underwent follow-up assessments. BMI training included voluntary desynchronization of ipsilesional EEG-sensorimotor rhythms triggering paretic upper-limb movements via robotic orthoses (experimental group, n = 16) or random orthoses movements (sham group, n = 12). Both groups received identical physiotherapy following BMI sessions and a home-based training program after intervention. Upper-limb motor assessment scores, electromyography (EMG), and functional magnetic resonance imaging (fMRI) were assessed before (Pre), immediately after (Post1), and 6 months after intervention (Post2). RESULTS: The experimental group presented with upper-limb Fugl-Meyer assessment (cFMA) scores significantly higher in Post2 (13.44 ± 1.96) as compared with the Pre session (11.16 ± 1.73; P = .015) and no significant changes between Post1 and Post2 sessions. The Sham group showed no significant changes on cFMA scores. Ashworth scores and EMG activity in both groups increased from Post1 to Post2. Moreover, fMRI-BOLD laterality index showed no significant difference from Pre or Post1 to Post2 sessions. CONCLUSIONS: BMI-based rehabilitation promotes long-lasting improvements in motor function of chronic stroke patients with severe paresis and represents a promising strategy in severe stroke neurorehabilitation.

A hybrid brain-machine interface based on EEG and EMG activity for the motor rehabilitation of stroke patients.

Including supplementary information from the brain or other body parts in the control of brain-machine interfaces (BMIs) has been recently proposed and investigated. Such enriched interfaces are referred to as hybrid BMIs (hBMIs) and have been proven to be more robust and accurate than regular BMIs for assistive and rehabilitative applications. Electromyographic (EMG) activity is one of the most widely utilized biosignals in hBMIs, as it provides a quite direct measurement of the motion intention of the user. Whereas most of the existing non-invasive EEG-EMG-hBMIs have only been subjected to offline testings or are limited to one degree of freedom (DoF), we present an EEG-EMG-hBMI that allows the simultaneous control of 7-DoFs of the upper limb with a robotic exoskeleton. Moreover, it establishes a biologically-inspired hierarchical control flow, requiring the active participation of central and peripheral structures of the nervous system. Contingent visual and proprioceptive feedback about the user's EEG and EMG activity is provided in the form of velocity modulation during functional task training. We believe that training with this closed-loop system may facilitate functional neuroplastic processes and eventually elicit a joint brain and muscle motor rehabilitation. Its usability is validated during a real-time operation session in a healthy participant and a chronic stroke patient, showing encouraging results for its application to a clinical rehabilitation scenario.

Residual Upper Arm Motor Function Primes Innervation of Paretic Forearm Muscles in Chronic Stroke after Brain-Machine Interface (BMI) Training.

BACKGROUND: Abnormal upper arm-forearm muscle synergies after stroke are poorly understood. We investigated whether upper arm function primes paralyzed forearm muscles in chronic stroke patients after Brain-Machine Interface (BMI)-based rehabilitation. Shaping upper arm-forearm muscle synergies may support individualized motor rehabilitation strategies. METHODS: Thirty-two chronic stroke patients with no active finger extensions were randomly assigned to experimental or sham groups and underwent daily BMI training followed by physiotherapy during four weeks. BMI sessions included desynchronization of ipsilesional brain activity and a robotic orthosis to move the paretic limb (experimental group, n = 16). In the sham group (n = 16) orthosis movements were random. Motor function was evaluated with electromyography (EMG) of forearm extensors, and upper arm and hand Fugl-Meyer assessment (FMA) scores. Patients performed distinct upper arm (e.g., shoulder flexion) and hand movements (finger extensions). Forearm EMG activity significantly higher during upper arm movements as compared to finger extensions was considered facilitation of forearm EMG activity. Intraclass correlation coefficient (ICC) was used to test inter-session reliability of facilitation of forearm EMG activity. RESULTS: Facilitation of forearm EMG activity ICC ranges from 0.52 to 0.83, indicating fair to high reliability before intervention in both limbs. Facilitation of forearm muscles is higher in the paretic as compared to the healthy limb (p<0.001). Upper arm FMA scores predict facilitation of forearm muscles after intervention in both groups (significant correlations ranged from R = 0.752, p = 0.002 to R = 0.779, p = 0.001), but only in the experimental group upper arm FMA scores predict changes in facilitation of forearm muscles after intervention (R = 0.709, p = 0.002; R = 0.827, p<0.001). CONCLUSIONS: Residual upper arm motor function primes recruitment of paralyzed forearm muscles in chronic stroke patients and predicts changes in their recruitment after BMI training. This study suggests that changes in upper arm-forearm synergies contribute to stroke motor recovery, and provides candidacy guidelines for similar BMI-based clinical practice.

Decoding upper limb residual muscle activity in severe chronic stroke.

OBJECTIVE: Stroke is a leading cause of long-term motor disability. Stroke patients with severe hand weakness do not profit from rehabilitative treatments. Recently, brain-controlled robotics and sequential functional electrical stimulation allowed some improvement. However, for such therapies to succeed, it is required to decode patients' intentions for different arm movements. Here, we evaluated whether residual muscle activity could be used to predict movements from paralyzed joints in severely impaired chronic stroke patients. METHODS: Muscle activity was recorded with surface-electromyography (EMG) in 41 patients, with severe hand weakness (Fugl-Meyer Assessment [FMA] hand subscores of 2.93 ± 2.7), in order to decode their intention to perform six different motions of the affected arm, required for voluntary muscle activity and to control neuroprostheses. Decoding of paretic and nonparetic muscle activity was performed using a feed-forward neural network classifier. The contribution of each muscle to the intended movement was determined. RESULTS: Decoding of up to six arm movements was accurate (>65%) in more than 97% of nonparetic and 46% of paretic muscles. INTERPRETATION: These results demonstrate that some level of neuronal innervation to the paretic muscle remains preserved and can be used to implement neurorehabilitative treatments in 46% of patients with severe paralysis and extensive cortical and/or subcortical lesions. Such decoding may allow these patients for the first time after stroke to control different motions of arm prostheses through muscle-triggered rehabilitative treatments.

Cortex integrity relevance in muscle synergies in severe chronic stroke.

BACKGROUND: Recent experimental evidence has indicated that the motor system coordinates muscle activations through a linear combination of muscle synergies that are specified at the spinal or brainstem networks level. After stroke upper limb impairment is characterized by abnormal patterns of muscle activations or synergies. OBJECTIVE: This study aimed at characterizing the muscle synergies in severely affected chronic stroke patients. Furthermore, the influence of integrity of the sensorimotor cortex on synergy modularity and its relation with motor impairment was evaluated. METHODS: Surface electromyography from 33 severely impaired chronic stroke patients was recorded during 6 bilateral movements. Muscle synergies were extracted and synergy patterns were correlated with motor impairment scales. RESULTS: Muscle synergies extracted revealed different physiological patterns dependent on the preservation of the sensorimotor cortex. Patients without intact sensorimotor cortex showed a high preservation of muscle synergies. On the contrary, patients with intact sensorimotor cortex showed poorer muscle synergies preservation and an increase in new generated synergies. Furthermore, the preservation of muscle synergies correlated positively with hand functionality in patients with intact sensorimotor cortex and subcortical lesions only. CONCLUSION: Our results indicate that severely paralyzed chronic stroke patient with intact sensorimotor cortex might sculpt new synergy patterns as a response to maladaptive compensatory strategies.

A new hand assessment instrument for severely affected stroke patients.

BACKGROUND: Standard assessment instruments cannot differentiate patients with minimal residual hand function after stroke. As a result, changes in motor recovery are difficult to document using currently-available tests. In a controlled study with chronic stroke patients without residual finger extension, a new hand function test has been developed. This instrument, called Broetz Hand Test (BzH), allows to assess small variations in hand function in severely paralyzed stoke patients. The instrument is easy to use, and was developed using principles of motor learning and behavioral assessment. METHODS: The instrument consists of seven daily life-oriented tasks, each of which asks for movement of the paralyzed hand. BzH of 20 patients after stroke was evaluated before and after a behavioral physiotherapy treatment. Sensitivity, inter-observer reliability, test-retest reliability and construct validity was calculated. RESULTS: Two-tailed paired-samples t-test before and after treatment demonstrated sufficient sensitivity. Mean agreement between the raters resulted in an excellent interrater-reliability. Test-retest reliability between the pre- and post-treatment scores was 0.9. The correlation between BzH and standard test scores was statistically significant and demonstrated sufficient validity. CONCLUSION: The BzH is a valid and reliable tool to assess changes in hand function in severely paralyzed patients after stroke.

Behavioral physiotherapy in post stroke rehabilitation.

INTRODUCTION: Behavioral aspects of motor learning such as definition and assessment of patient-centered goals, specific motivation, training in the patients' environment, autonomous training and generalization of newly learned skills to daily life are not an explicit part of physiotherapy in neurorehabilitation. BEHAVIORAL PHYSIOTHERAPY: Specific goals are defined and applied in a step by step manner. Exercises and application in daily life were trained and anticipated as a "self control cue" for the following week. Motivation was sustained via supervision, feedback after successful trials and reward. Exercises have to occure at a daily basis and have to be implemented in everyday life. CASE DESCRIPTION: A 54 year old man who suffered cerebral bleeding with left hemiparesis 25 years ago. We report goal attainment, change of symptoms and walking capacities over a period of 18 months. RESULTS: Back pain and knee pain reduced to zero, rhythmic walking, walking speed increased, left leg less resistance, running possible. DISCUSSION: The here described principles of behavioral physiotherapy are crucial for successful outcome in extremely stable and persistent consequences of stroke. Studies with more patients are needed to strengthen our hypothesis.

Brain-machine interface in chronic stroke rehabilitation: a controlled study.

OBJECTIVE: Chronic stroke patients with severe hand weakness respond poorly to rehabilitation efforts. Here, we evaluated efficacy of daily brain-machine interface (BMI) training to increase the hypothesized beneficial effects of physiotherapy alone in patients with severe paresis in a double-blind sham-controlled design proof of concept study. METHODS: Thirty-two chronic stroke patients with severe hand weakness were randomly assigned to 2 matched groups and participated in 17.8 ± 1.4 days of training rewarding desynchronization of ipsilesional oscillatory sensorimotor rhythms with contingent online movements of hand and arm orthoses (experimental group, n = 16). In the control group (sham group, n = 16), movements of the orthoses occurred randomly. Both groups received identical behavioral physiotherapy immediately following BMI training or the control intervention. Upper limb motor function scores, electromyography from arm and hand muscles, placebo-expectancy effects, and functional magnetic resonance imaging (fMRI) blood oxygenation level-dependent activity were assessed before and after intervention. RESULTS: A significant group × time interaction in upper limb (combined hand and modified arm) Fugl-Meyer assessment (cFMA) motor scores was found. cFMA scores improved more in the experimental than in the control group, presenting a significant improvement of cFMA scores (3.41 ± 0.563-point difference, p = 0.018) reflecting a clinically meaningful change from no activity to some in paretic muscles. cFMA improvements in the experimental group correlated with changes in fMRI laterality index and with paretic hand electromyography activity. Placebo-expectancy scores were comparable for both groups. INTERPRETATION: The addition of BMI training to behaviorally oriented physiotherapy can be used to induce functional improvements in motor function in chronic stroke patients without residual finger movements and may open a new door in stroke neurorehabilitation.

Combination of brain-computer interface training and goal-directed physical therapy in chronic stroke: a case report.

BACKGROUND: There is no accepted and efficient rehabilitation strategy to reduce focal impairments for patients with chronic stroke who lack residual movements. METHODS: A 67-year-old hemiplegic patient with no active finger extension was trained with a brain-computer interface (BCI) combined with a specific daily life-oriented physiotherapy. The BCI used electrical brain activity (EEG) and magnetic brain activity (MEG) to drive an orthosis and a robot affixed to the patient's affected upper extremity, which enabled him to move the paralyzed arm and hand driven by voluntary modulation of micro-rhythm activity. In addition, the patient practiced goal-directed physiotherapy training. Over 1 year, he completed 3 training blocks. Arm motor function, gait capacities (using Fugl-Meyer Assessment, Wolf Motor Function Test, Modified Ashworth Scale, 10-m walk speed, and goal attainment score), and brain reorganization (functional MRI, MEG) were repeatedly assessed. RESULTS: The ability of hand and arm movements as well as speed and safety of gait improved significantly (mean 46.6%). Improvement of motor function was associated with increased micro-oscillations in the ipsilesional motor cortex. CONCLUSION: This proof-of-principle study suggests that the combination of BCI training with goal-directed, active physical therapy may improve the motor abilities of chronic stroke patients despite apparent initial paralysis.

Lumbar disk prolapse: response to mechanical physiotherapy in the absence of changes in magnetic resonance imaging. Report of 11 cases.

BACKGROUND: Lumbar disk prolapses are among the most common neurological conditions. In this open study, we asked whether repeated end-range spinal movements (McKenzie method) as physiotherapy in patients with lumbar disk prolapse induce early changes in location, size and signal intensity of lumbar disc material detectable by magnetic resonance imaging (MRI). We compared clinical with radiographic changes. The clinical efficacy of mechanical physiotherapy according to the McKenzie method within 5 days was documented. METHODS: Eleven consecutive patients with lumbar disk prolapse were included. Patients were treated with repeated end-range spinal movements and MRI was performed before and after 2-5 treatments. RESULTS: All patients achieved a reduction in symptoms and signs of disk prolapse during and after these procedures but none showed any change in the MRI features of the prolapses. CONCLUSIONS: Beneficial effects of specific mechanical physiotherapy in patients with radicular syndromes from lumbar disk prolapse are not paralleled by changes in the MRI appearance of the prolapses. Alternative explanations for the early clinical responses in some patients with lumbar disc prolapse treated according to the McKenzie method must be sought.

Radicular and nonradicular back pain in Parkinson's disease: a controlled study.

Postural abnormalities and increased muscle tone in Parkinson's disease (PD) may cause back pain. In this controlled study, we analyzed features of back pain in PD patients. The prevalence of back pain was 74% in PD patients (n = 101) when compared with 27% in control patients (n = 132; P < 0.0001, fisher's exact test), but did not correlate with disease severity or duration. The mean back pain intensity (visual analog scale of 0-10) was 4.3 for PD patients, and 1.3 for controls. Both radicular and nonradicular types of back pain were more frequent, and back pain caused more impairment in PD patients. However, it is noteworthy that the PD patients in our study did not receive more pain medication than control patients. This suggests that back pain in PD patients is often neglected and insufficiently treated. Our results argue for the routine evaluation of back pain in every patient suffering from PD.

Leg orientation as a clinical sign for pusher syndrome.

BACKGROUND: Effective control of (upright) body posture requires a proper representation of body orientation. Stroke patients with pusher syndrome were shown to suffer from severely disturbed perception of own body orientation. They experience their body as oriented 'upright' when actually tilted by nearly 20 degrees to the ipsilesional side. Thus, it can be expected that postural control mechanisms are impaired accordingly in these patients. Our aim was to investigate pusher patients' spontaneous postural responses of the non-paretic leg and of the head during passive body tilt. METHODS: A sideways tilting motion was applied to the trunk of the subject in the roll plane. Stroke patients with pusher syndrome were compared to stroke patients not showing pushing behaviour, patients with acute unilateral vestibular loss, and non brain damaged subjects. RESULTS: Compared to all groups without pushing behaviour, the non-paretic leg of the pusher patients showed a constant ipsiversive tilt across the whole tilt range for an amount which was observed in the non-pusher subjects when they were tilted for about 15 degrees into the ipsiversive direction. CONCLUSION: The observation that patients with acute unilateral vestibular loss showed no alterations of leg posture indicates that disturbed vestibular afferences alone are not responsible for the disordered leg responses seen in pusher patients. Our results may suggest that in pusher patients a representation of body orientation is disturbed that drives both conscious perception of body orientation and spontaneous postural adjustment of the non-paretic leg in the roll plane. The investigation of the pusher patients' leg-to-trunk orientation thus could serve as an additional bedside tool to detect pusher syndrome in acute stroke patients.

"Pusher syndrome" following cortical lesions that spare the thalamus.

Stroke patients with "pusher syndrome" show severe misperception of their own upright body orientation although visual-vestibular processing is almost intact. This dissociation argues for a second graviceptive system in humans for the perception of body orientation. Recent studies revealed that the posterior thalamus is an important part of this system. The present investigation aimed to study the cortical representation of this system beyond the thalamus. We evaluated 45 acute patients with and without contraversive pushing following left-or right-sided cortical lesions sparing the thalamus. In both hemispheres, the simple lesion overlap associated with contraversive pushing typically centered on the insular cortex and parts of the postcentral gyrus. The comparison between pusher patients and controls who were matched with respect to age, lesion size, and the frequency of spatial neglect, aphasia and visual field defects revealed only very small regions that were specific for the pusher patients with cortical damage sparing the thalamus. Obviously, the cortical structures representing our control of upright body orientation are in close anatomical proximity to those areas that induce aphasia in the left hemisphere and spatial neglect in the right hemisphere when lesioned. We conclude that in addition to the subcortical area previously identified in the posterior thalamus, parts of the insula and postcentral gyrus appear to contribute at cortical level to the processing of the afferent signals mediating the graviceptive information about upright body orientation.

Posterior thalamic hemorrhage induces "pusher syndrome".

BACKGROUND: Recent findings argue for a pathway in humans for sensing the orientation of gravity and controlling upright body posture, separate from the one for orientation perception of the visual world. Stroke patients with contraversive pushing were shown to experience their body as oriented upright when actually tilted about 20 degrees to the ipsilesional side, in spite of normal visual-vestibular functioning. A recent study suggested the involvement of posterolateral thalamus typically associated with the disorder. OBJECTIVE: To evaluate the relationship between pushing behavior and thalamic function. METHODS: Over a 3-year period the authors prospectively investigated 40 patients with left- or right-sided thalamic strokes. RESULTS: Twenty-eight percent showed contraversive pushing. The authors found a strong relationship between etiology, vascular territory, lesion size, and neurologic disorders associated with contraversive pushing. Pusher patients had larger lesions that typically were caused by hemorrhage (vs infarcts) located in the posterior thalamus (vs anterior thalamic lesions in those patients without pushing behavior). A paresis of the contralesional extremities was more frequent and more severe in pusher patients. Further, these patients showed more additional spatial neglect with right thalamic lesions, while they tended to be more aphasic with left thalamic lesions. CONCLUSIONS: Posterior thalamus seems to be fundamentally involved in our control of upright body posture. Higher pressure, swelling, and other secondary pathologic processes associated with posterior thalamic hemorrhage (vs thalamic infarction) may provoke contraversive pushing in combination with additional neurologic symptoms.

Understanding and treating "pusher syndrome".

"Pusher syndrome" is a clinical disorder following left or right brain damage in which patients actively push away from the nonhemiparetic side, leading to a loss of postural balance. The mechanism underlying this disorder and its related anatomy have only recently been identified. Investigation of patients with severe pushing behavior has shown that perception of body posture in relation to gravity is altered. The patients experience their body as oriented "upright" when the body actually is tilted to the side of the brain lesion (to the ipsilesional side). In contrast, patients with pusher syndrome show no disturbed processing of visual and vestibular inputs determining visual vertical. These new insights have allowed the authors to suggest a new physical therapy approach for patients with pusher syndrome where the visual control of vertical upright orientation, which is undisturbed in these patients, is the central element of intervention.