Neurophysiological underpinnings of an intensive protocol for upper limb motor recovery in subacute and chronic stroke patients

Background: Upper limb (UL) motor impairment following stroke is a leading cause of functional limitations in activities of daily living. Robot-assisted therapy supports rehabilitation, but how its efficacy and the underlying neural mechanisms depend on the time after stroke is yet to be assessed. Aim: We investigated the response to an intensive protocol of robot-assisted rehabilitation in sub-acute and chronic stroke patients, by analyzing the underlying changes in clinical scores, electroencephalography (EEG) and end-effector kinematics. We aimed at identifying neural correlates of the participants' upper limb motor function recovery, following an intensive 2-week rehabilitation protocol. Design: Prospective cohort study. Setting: Inpatients and outpatients from the Neurorehabilitation Unit of Pisa University Hospital, Italy. Population: Sub-acute and chronic stroke survivors. Methods: Thirty-one stroke survivors (14 sub-acute, 17 chronic) with mild-to-moderate UL paresis were enrolled. All participants underwent ten rehabilitative sessions of task-oriented exercises with a planar end-effector robotic device. All patients were evaluated with the Fugl-Meyer Assessment Scale and the Wolf Motor Function Test, at recruitment (T0), end-of-treatment (T1), and one-month follow-up (T2). Along with clinical scales, kinematic parameters and quantitative EEG were collected for each patient. Kinematics metrics were related to velocity, acceleration and smoothness of the movement. Relative power in four frequency bands was extracted from the EEG signals. The evolution over time of kinematic and EEG features was analyzed, in correlation with motor recovery. Results: Both groups displayed significant gains in motility after treatment. Sub-acute patients displayed more pronounced clinical improvements, significant changes in kinematic parameters, and a larger increase in Beta-band in the motor area of the affected hemisphere. In both groups these improvements were associated to a decrease in the Delta-band of both hemispheres. Improvements were retained at T2. Conclusions: The intensive two-week rehabilitation protocol was effective in both chronic and sub-acute patients, and improvements in the two groups shared similar dynamics. However, stronger cortical and behavioral changes were observed in sub-acute patients suggesting different reorganizational patterns. Clinical rehabilitation impact: This study paves the way to personalized approaches to UL motor rehabilitation after stroke, as highlighted by different neurophysiological modifications following recovery in subacute and chronic stroke patients

A Neurally Inspired Robotic Control Algorithm for Gait Rehabilitation in Hemiplegic Stroke Patients

Abstract-Cerebrovascular accident or stroke is one of the major brain impairments that affects numerous people globally. After a unilateral stroke, sensory motor damages contralateral to the brain lesion occur in many patients. As a result, gait remains impaired and asymmetric. This paper describes and simulates a novel closed loop algorithm designed for the control of a lower limb exoskeleton for post-stroke rehabilitation. The algorithm has been developed to control a lower limb exoskeleton including actuators for the hip and knee joints, and feedback sensors for the measure of joint angular excursions. It has been designed to control and correct the gait cycle of the affected leg using kinematics information from the unaffected one. In particular, a probabilistic particle filter like algorithm has been used at the top-level control to modulate gait velocity and the joint angular excursions. Simulation results show that the algorithm is able to correct and control velocity of the affected side restoring phase synchronization between the legs

Deep learning-based BCI for gait decoding from EEG with LSTM recurrent neural network

Objective.Mobile Brain/Body Imaging (MoBI) frameworks allowed the research community to find evidence of cortical involvement at walking initiation and during locomotion. However, the decoding of gait patterns from brain signals remains an open challenge. The aim of this work is to propose and validate a deep learning model to decode gait phases from Electroenchephalography (EEG).Approach.A Long-Short Term Memory (LSTM) deep neural network has been trained to deal with time-dependent information within brain signals during locomotion. The EEG signals have been preprocessed by means of Artifacts Subspace Reconstruction (ASR) and Reliable Independent Component Analysis (RELICA) to ensure that classification performance was not affected by movement-related artifacts.Main results.The network was evaluated on the dataset of 11 healthy subjects walking on a treadmill. The proposed decoding approach shows a robust reconstruction (AUC > 90%) of gait patterns (i.e. swing and stance states) of both legs together, or of each leg independently.Significance.Our results support for the first time the use of a memory-based deep learning classifier to decode walking activity from non-invasive brain recordings. We suggest that this classifier, exploited in real time, can be a more effective input for devices restoring locomotion in impaired people

Cortico-muscular connectivity is modulated by passive and active Lokomat-assisted Gait

The effects of robotic-assisted gait (RAG) training, besides conventional therapy, on neuroplasticity mechanisms and cortical integration in locomotion are still uncertain. To advance our knowledge on the matter, we determined the involvement of motor cortical areas in the control of muscle activity in healthy subjects, during RAG with Lokomat, both with maximal guidance force (100 GF—passive RAG) and without guidance force (0 GF—active RAG) as customary in rehabilitation treatments. We applied a novel cortico-muscular connectivity estimation procedure, based on Partial Directed Coherence, to jointly study source localized EEG and EMG activity during rest (standing) and active/passive RAG. We found greater cortico-cortical connectivity, with higher path length and tendency toward segregation during rest than in both RAG conditions, for all frequency bands except for delta. We also found higher cortico-muscular connectivity in distal muscles during swing (0 GF), and stance (100 GF), highlighting the importance of direct supraspinal control to maintain balance, even when gait is supported by a robotic exoskeleton. Source-localized connectivity shows that this control is driven mainly by the parietal and frontal lobes. The involvement of many cortical areas also in passive RAG (100 GF) justifies the use of the 100 GF RAG training for neurorehabilitation, with the aim of enhancing cortical-muscle connections and driving neural plasticity in neurological patients

Discrimination of Walking and Standing from Entropy of EEG Signals and Common Spatial Patterns

Recently, the complexity analysis of brain activity has shown the possibility to provide additional information to discriminate between rest and motion in real-time. In this work, we propose a novel entropy-based machine learning method to classify between standing and walking conditions from the sole brain activity. The Shannon entropy has been used as a complexity measure of electroencephalography (EEG) signals and subject-specific features for classification have been selected by Common Spatial Patterns (CSP) filter. Exploiting these features with a linear classifier, we achieved > 85% of classification accuracy over a long period (approximate to 25 min) of standing and treadmill walking on 11 healthy subjects. Moreover, we implemented the proposed approach to successfully discriminate in real-time between standing and over-ground walking on one healthy subject. We suggest that the reliable discrimination of rest against walking conditions achieved by the proposed method may be exploited to have more stable control of devices to restore locomotion, avoiding unpredictable and dangerous behaviors due to the delivery of undesired control commands.TN

Hybrid Human-Machine Interface for Gait Decoding Through Bayesian Fusion of EEG and EMG Classifiers

Despite the advances in the field of brain computer interfaces (BCI), the use of the sole electroencephalography (EEG) signal to control walking rehabilitation devices is currently not viable in clinical settings, due to its unreliability. Hybrid interfaces (hHMIs) represent a very recent solution to enhance the performance of single-signal approaches. These are classification approaches that combine multiple human-machine interfaces, normally including at least one BCI with other biosignals, such as the electromyography (EMG). However, their use for the decoding of gait activity is still limited. In this work, we propose and evaluate a hybrid human-machine interface (hHMI) to decode walking phases of both legs from the Bayesian fusion of EEG and EMG signals. The proposed hHMI significantly outperforms its single-signal counterparts, by providing high and stable performance even when the reliability of the muscular activity is compromised temporarily (e.g., fatigue) or permanently (e.g., weakness). Indeed, the hybrid approach shows a smooth degradation of classification performance after temporary EMG alteration, with more than 75% of accuracy at 30% of EMG amplitude, with respect to the EMG classifier whose performance decreases below 60% of accuracy. Moreover, the fusion of EEG and EMG information helps keeping a stable recognition rate of each gait phase of more than 80% independently on the permanent level of EMG degradation. From our study and findings from the literature, we suggest that the use of hybrid interfaces may be the key to enhance the usability of technologies restoring or assisting the locomotion on a wider population of patients in clinical applications and outside the laboratory environment