Dynamics of brain connectivity after stroke

PURPOSE: Recovery from a stroke is a dynamic time-dependent process with the central nervous system reorganizing to accommodate for the impact of the injury. The purpose of this paper is to review recent longitudinal studies of changes in brain connectivity after stroke. METHOD: A systematic review of research papers reporting functional or effective connectivity at two or more time points in stroke patients. RESULTS: Stroke leads to an early reduction of connectivity in the motor network. With recovery time, the connectivity increases and can reach the same levels as in healthy participants. The increase in connectivity is correlated with functional motor gains. A new, more randomized pattern of connectivity may then emerge in the longer term. In some instances, a pattern of increased connectivity even higher than in healthy controls can be observed, related either to a specific time point or to a specific neural structure. Rehabilitation interventions can help improve connectivity between specific regions. CONCLUSIONS: Motor network connectivity undergoes reorganization during recovery from a stroke and can be related to behavioural recovery. Detailed analysis of changes in connectivity pattern may enable a better understanding of adaptation to a stroke and how compensatory mechanisms in the brain may be supported by rehabilitation

Proprioceptive feedback facilitates motor imagery-related operant learning of sensorimotor β-band modulation

Motor imagery (MI) activates the sensorimotor system independent of actual movements and might be facilitated by neurofeedback. Knowledge on the interaction between feedback modality and the involved frequency bands during MI-related brain self-regulation is still scarce. Previous studies compared the cortical activity during the MI task with concurrent feedback (MI with feedback condition) to cortical activity during the relaxation task where no feedback was provided (relaxation without feedback condition). The observed differences might, therefore, be related to either the task or the feedback. A proper comparison would necessitate studying a relaxation condition with feedback and a MI task condition without feedback as well. Right-handed healthy subjects performed two tasks, i.e., MI and relaxation, in alternating order. Each of the tasks (MI vs. relaxation) was studied with and without feedback. The respective event-driven oscillatory activity, i.e., sensorimotor desynchronization (during MI) or synchronization (during relaxation), was rewarded with contingent feedback. Importantly, feedback onset was delayed to study the task-related cortical activity in the absence of feedback provision during the delay period. The reward modality was alternated every 15 trials between proprioceptive and visual feedback. Proprioceptive input was superior to visual input to increase the range of task-related spectral perturbations in the α- and β-band, and was necessary to consistently achieve MI-related sensorimotor desynchronization (ERD) significantly below baseline. These effects occurred in task periods without feedback as well. The increased accuracy and duration of learned brain self-regulation achieved in the proprioceptive condition was specific to the β-band. MI-related operant learning of brain self-regulation is facilitated by proprioceptive feedback and mediated in the sensorimotor β-band

Bridging the gap between emotion and joint action

Our daily human life is filled with a myriad of joint action moments, be it children playing, adults working together (i.e., team sports), or strangers navigating through a crowd. Joint action brings individuals (and embodiment of their emotions) together, in space and in time. Yet little is known about how individual emotions propagate through embodied presence in a group, and how joint action changes individual emotion. In fact, the multi-agent component is largely missing from neuroscience-based approaches to emotion, and reversely joint action research has not found a way yet to include emotion as one of the key parameters to model socio-motor interaction. In this review, we first identify the gap and then stockpile evidence showing strong entanglement between emotion and acting together from various branches of sciences. We propose an integrative approach to bridge the gap, highlight five research avenues to do so in behavioral neuroscience and digital sciences, and address some of the key challenges in the area faced by modern societies

Enhancement of Robot-Assisted Rehabilitation Outcomes of Post-Stroke Patients Using Movement-Related Cortical Potential

Post-stroke rehabilitation is essential for stroke survivors to help them regain independence and to improve their quality of life. Among various rehabilitation strategies, robot-assisted rehabilitation is an efficient method that is utilized more and more in clinical practice for motor recovery of post-stroke patients. However, excessive assistance from robotic devices during rehabilitation sessions can make patients perform motor training passively with minimal outcome. Towards the development of an efficient rehabilitation strategy, it is necessary to ensure the active participation of subjects during training sessions. This thesis uses the Electroencephalography (EEG) signal to extract the Movement-Related Cortical Potential (MRCP) pattern to be used as an indicator of the active engagement of stroke patients during rehabilitation training sessions. The MRCP pattern is also utilized in designing an adaptive rehabilitation training strategy that maximizes patients’ engagement. This project focuses on the hand motor recovery of post-stroke patients using the AMADEO rehabilitation device (Tyromotion GmbH, Austria). AMADEO is specifically developed for patients with fingers and hand motor deficits. The variations in brain activity are analyzed by extracting the MRCP pattern from the acquired EEG data during training sessions. Whereas, physical improvement in hand motor abilities is determined by two methods. One is clinical tests namely Fugl-Meyer Assessment (FMA) and Motor Assessment Scale (MAS) which include FMA-wrist, FMA-hand, MAS-hand movements, and MAS-advanced hand movements’ tests. The other method is the measurement of hand-kinematic parameters using the AMADEO assessment tool which contains hand strength measurements during flexion (force-flexion), and extension (force-extension), and Hand Range of Movement (HROM)

Die Bedeutung kognitiver Belastung und adaptiver Schwierigkeitsanpassung für Neurofeedback-basiertes Training

In der vorliegenden Arbeit wurden die grundlegenden Eigenschaften und Wirkungen eines Brain-Machine-Interfaces (BMI), das im EEG gemessene Hirnaktivität in Bewegungen einer Handorthese umsetzt, bei gesunden Probanden untersucht. In der ersten Studie wurden die kortikalen Netzwerke von Probanden mittels EEG untersucht, bevor sie unterschiedliche motorische Aufgaben durchführten: Bewegungsvorstellung (Motor Imagery, MI), tatsächliche Bewegungen (Motor Execution, ME) und die Benutzung eines BMI (d.h. MI mit Feedback durch die Handorthese). Es konnte gezeigt werden, dass Ruhe EEG-Netzwerke die anschließende Fähigkeit der Probanden zu MI, ME und BMI-Anwendung vorhersagen können. Dabei überlappen sich die kortikalen Netzwerke für MI und ME zum Teil, zeigen jedoch auch relevante Unterschiede. In diesem Kontext kann die BMI-Anwendung die Netzwerke und Fähigkeiten von MI und ME überbrücken. In der zweiten Studie wurde das BMI Training mit einem etablierten EMG-basierten Neurofeedback Training verglichen, um die jeweilige kognitive Belastung zu ermitteln. Dabei unterschied sich die kognitive Belastung des BMI Feedbacks vom EMG Feedback und konnte insbesondere zu Frustration führen. Das Frustrationserleben korreliert aber über die verschiedenen Feedback Aufgaben hinweg und legt daher eine spezifische Eigenschaft des Teilnehmers (personal trait) nahe. Darüber hinaus konnte die kognitive Belastung unabhängig von der jeweiligen Aufgabe anhand kortikaler Netzwerke im EEG sowohl in Ruhe als auch während der Aufgabe bestimmt werden. In der dritten Studie erfolgte schließlich eine Schwierigkeits-Adaptation auf der Basis der kognitiven Belastung der Teilnehmer. Die von den Teilnehmern berichtete kognitive Belastung korrelierte dabei mit dem Schwierigkeitsgrad des BMI Trainings. Eine adaptive Schwierigkeitsanpassung des BMI erhöhte schließlich die Leistung und reduzierte die kognitive Belastung der Teilnehmer. Insgesamt wurden mit diesen Probandenstudien die Voraussetzungen geschaffen, ein adaptives Neurofeedback Training zu entwickeln, das langfristig in der Rehabilitation von Schlaganfallpatienten mit motorischen Einschränkungen der Hand eingesetzt werden kann

User Experience May be Producing Greater Heart Rate Variability than Motor Imagery Related Control Tasks during the User-System Adaptation in Brain-Computer Interfaces

Brain-computer interface (BCI) is technology that is developing fast, but it remains inaccurate, unreliable and slow due to the difficulty to obtain precise information from the brain. Consequently, the involvement of other biosignals to decode the user control tasks has risen in importance. A traditional way to operate a BCI system is via motor imagery (MI) tasks. As imaginary movements activate similar cortical structures and vegetative mechanisms as a voluntary movement does, heart rate variability (HRV) has been proposed as a parameter to improve the detection of MI related control tasks. However, HR is very susceptible to body needs and environmental demands, and as BCI systems require high levels of attention, perceptual processing and mental workload, it is important to assess the practical effectiveness of HRV. The present study aimed to determine if brain and heart electrical signals (HRV) are modulated by MI activity used to control a BCI system, or if HRV is modulated by the user perceptions and responses that result from the operation of a BCI system (i.e., user experience). For this purpose, a database of 11 participants who were exposed to eight different situations was used. The sensory-cognitive load (intake and rejection tasks) was controlled in those situations. Two electrophysiological signals were utilized: electroencephalography and electrocardiography. From those biosignals, event-related (de-)synchronization maps and event-related HR changes were respectively estimated. The maps and the HR changes were cross-correlated in order to verify if both biosignals were modulated due to MI activity. The results suggest that HR varies according to the experience undergone by the user in a BCI working environment, and not because of the MI activity used to operate the system

Comparison of Brain Activation during Motor Imagery and Motor Movement Using fNIRS

Motor-activity-related mental tasks are widely adopted for brain-computer interfaces (BCIs) as they are a natural extension of movement intention, requiring no training to evoke brain activity. The ideal BCI aims to eliminate neuromuscular movement, making motor imagery tasks, or imagined actions with no muscle movement, good candidates. This study explores cortical activation differences between motor imagery and motor execution for both upper and lower limbs using functional near-infrared spectroscopy (fNIRS). Four simple finger- or toe-tapping tasks (left hand, right hand, left foot, and right foot) were performed with both motor imagery and motor execution and compared to resting state. Significant activation was found during all four motor imagery tasks, indicating that they can be detected via fNIRS. Motor execution produced higher activation levels, a faster response, and a different spatial distribution compared to motor imagery, which should be taken into account when designing an imagery-based BCI. When comparing left versus right, upper limb tasks are the most clearly distinguishable, particularly during motor execution. Left and right lower limb activation patterns were found to be highly similar during both imagery and execution, indicating that higher resolution imaging, advanced signal processing, or improved subject training may be required to reliably distinguish them

Brain-computer interface technology and neuroelectrical imaging to improve motor recovery after stroke

Stroke is defined as a focal lesion in the brain caused by acute ischemia or hemorrhage. The events that characterize acute stroke as well as the spontaneous recovery process occurring in the subacute phase, demonstrate that the focal damage affects remote interconnected areas. On the other hand, interconnected areas largely contribute to reorganization of the central nervous system (CNS) along the recovery process (plasticity) throughout compensatory or restorative mechanisms which can also lead to unwanted effects (maladaptive plasticity). Such post-stroke brain reorganization occurring spontaneously or within a rehabilitation program, is the object of wide literature in the fields of neuroimaging and neurophysiology. Brain-Computer Interfaces (BCIs) allow recognition, monitoring and reinforcement of specific brain activities as recorded eg. via electroencephalogram (EEG) and use such brain activity to control external devices via a computer. Sensorimotor rhythm (SMR) based BCIs exploit the modulation occurring in the EEG in response to motor imagery (MI) tasks: the subject is asked to perform MI of eg. left or right hand in order to control a cursor on a screen. In the context of post-stroke motor rehabilitation, such recruitment of brain activity within the motor system through MI can be used to harness brain reorganization towards a better functional outcome. Since 2009 my research activity has been focused mainly on BCI applications for upper limb motor rehabilitation after stroke within national (Ministry of Health) and international (EU) projects. I conducted (or participated to) several basic and clinical studies involving both healthy subjects and stroke patients and employing a combination of neurophysiological techniques (EEG, transcranial magnetic stimulation – TMS) and BCI technology (De Vico Fallani et al., 2013; Kaiser et al., 2012; Morone et al., 2015; Pichiorri et al., 2011). Such studies culminated in a randomized controlled trial (RCT) conducted on subacute stroke patients in which we demonstrated that a one-month training with a BCI system, which was specifically designed to support upper limb rehabilitation after stroke, significantly improved functional outcome (upper limb motor function) in the target population. Moreover, we observed changes in brain activity and connectivity (from high-density EEG recordings) occurring in motor related frequency ranges that significantly correlated to the functional outcome in the target group (Pichiorri et al., 2015). Following these promising results, my activity proceeded along two main pathways during the PhD course. On one hand, efforts were made ameliorate the prototypal BCI system used in (Pichiorri et al., 2015); the current system (called Promotœr) is an all-in-one BCI training station with several improvements in usability for both the patient and the therapist (it is easier to use, employs wireless EEG system with reduced number of electrodes) (Colamarino et al., 2017a,b). The Promotœr system is currently employed in add-on to standard rehabilitation therapy in patients admitted at Fondazione Santa Lucia. Preliminary results are available on chronic stroke patients, partially retracing those obtained in the subacute phase (Pichiorri et al., 2015) as well as explorative reports on patients with upper limb motor deficit of central origin other than stroke (eg. spinal cord injury at the cervical level). In the last year, I submitted research projects related to the Promotœr system to private and public institutions. These projects foresee i) the addition of a proprioceptive feedback to the current visual one by means of Functional Electrical Stimulation (FES) ii) online evaluation of residual voluntary movement as recorded via electromyography (EMG), and iii) improvements in the BCI control features to integrate concepts derived from recent advancements in brain connectivity. On these themes, I recently obtained a grant from a private Swedish foundation. On the other hand, I conducted further analyses of data collected in the RCT (Pichiorri et al., 2015) to identify possible neurophysiological markers of good motor recovery. Specifically, I focused on interhemispheric connectivity (EEG derived) and its correlation with the integrity of the corticospinal tract (as assessed by TMS) and upper limb function (measured with clinical scales) in subacute stroke patients. The results of these analyses were recently published on an international peer-reviewed journal (Pichiorri et al., 2018). In the first chapter of this thesis, I will provide an updated overview on BCI application in neurorehabilitation (according to the current state-of-the-art). The content of this chapter is part of a wider book chapter, currently in press in Handbook of Clinical Neurology (Pichiorri and Mattia, in press). In the second chapter, I will report on the status of BCI applications for motor rehabilitation of the upper limb according to the approach I developed along my research activity, including ongoing projects and prliminary findings. In the third chapter I will present the results of a neurophysiological study on subacute stroke patients, exploring EEG derived interhemispheric connectivity as a possible neurophysiological correlate of corticospinal tract integrity and functional impairment of the upper limb. Overall this work aims to outline the current and potential role of BCI technology and EEG based neuroimaging in post-stroke rehabilitation mainly in relation to upper limb motor function, nonetheless touching upon possible different applications and contexts in neighboring research fields