Silvestro Micera

A critical review of interfaces with the peripheral nervous system for the control of neuroprostheses and hybrid bionic systems

Abstract  Considerable scientific and technological efforts have been devoted to develop neuroprostheses and hybrid bionic systems that link the human nervous system with electronic or robotic prostheses, with the main aim of restoring motor and sensory functions in disabled patients. A number of neuroprostheses use interfaces with peripheral nerves or muscles for neuromuscular stimulation and signal recording. Herein, we provide a critical overview of the peripheral interfaces available and trace their use from research to clinical application in controlling artificial and robotic prostheses. The first section reviews the different types of non‐invasive and invasive electrodes, which include surface and muscular electrodes that can record EMG signals from and stimulate the underlying or implanted muscles. Extraneural electrodes, such as cuff and epineurial electrodes, provide simultaneous interface with many axons in the nerve, whereas intrafascicular, penetrating, and regenerative electrodes may contact small groups of axons within a nerve fascicle. Biological, technological, and material science issues are also reviewed relative to the problems of electrode design and tissue injury. The last section reviews different strategies for the use of information recorded from peripheral interfaces and the current state of control neuroprostheses and hybrid bionic systems.

Restoring Voluntary Control of Locomotion after Paralyzing Spinal Cord Injury

Regaining Limb Movement Despite many years of intensive research, there is still an urgent need for novel treatments to help patients restore motor function after spinal cord injuries. van den Brand et al. (p. 1182) produced left and right hemisections at different levels of the rat thoracic spinal cord to cause complete hind limb paralysis mimicking the situation in humans with spinal cord injury. Systemic application of pharmacological agents, combined with a multisystem rehabilitation program including a robotic postural neuroprosthesis, restored voluntary movements of both hind limbs. A rehabilitation program involving robotic neuroprosthetics restores previously paralyzed hindlimb function. Half of human spinal cord injuries lead to chronic paralysis. Here, we introduce an electrochemical neuroprosthesis and a robotic postural interface designed to encourage supraspinally mediated movements in rats with paralyzing lesions. Despite the interruption of direct supraspinal pathways, the cortex regained the capacity to transform contextual information into task-specific commands to execute refined locomotion. This recovery relied on the extensive remodeling of cortical projections, including the formation of brainstem and intraspinal relays that restored qualitative control over electrochemically enabled lumbosacral circuitries. Automated treadmill-restricted training, which did not engage cortical neurons, failed to promote translesional plasticity and recovery. By encouraging active participation under functional states, our training paradigm triggered a cortex-dependent recovery that may improve function after similar injuries in humans.

Restoring Natural Sensory Feedback in Real-Time Bidirectional Hand Prostheses

A multigrasp, bidirectional hand prosthesis delivers dynamic sensory feedback, allowing a user with a hand amputation to achieve fine grasping force control and realistic object sensing. An Artificial Hand’s Sense of Touch To feel the hard curvature of a baseball or the soft cylinder that is a soda can—these sensations we often take for granted. But amputees with a prosthetic arm know only that they are holding an object, the shape and stiffness discernible only by eye or from experience. Toward a more sophisticated prosthetic that can “feel” an object, Raspopovic and colleagues incorporated a feedback system connected to the amputee’s arm nerves, which delivers sensory information in real time. The authors connected electrodes in the arm nerves to sensors in two fingers of the prosthetic hand. To “feel” an object, the electrodes delivered electrical stimuli to the nerves that were proportional to the finger sensor readouts. To grasp an object and perform other motor commands, muscle signals were decoded. This bidirectional hand prosthetic was tested in a single amputee who was blindfolded and acoustically shielded to assure that sound and vision were not being used to manipulate objects. In more than 700 trials, the subject showed that he could modulate force and grasp and identify physical characteristics of different types of objects, such as cotton balls, an orange, and a piece of wood. Such sensory feedback with precise control over a hand prosthetic would allow amputees to more freely and naturally explore their environments. Hand loss is a highly disabling event that markedly affects the quality of life. To achieve a close to natural replacement for the lost hand, the user should be provided with the rich sensations that we naturally perceive when grasping or manipulating an object. Ideal bidirectional hand prostheses should involve both a reliable decoding of the user’s intentions and the delivery of nearly “natural” sensory feedback through remnant afferent pathways, simultaneously and in real time. However, current hand prostheses fail to achieve these requirements, particularly because they lack any sensory feedback. We show that by stimulating the median and ulnar nerve fascicles using transversal multichannel intrafascicular electrodes, according to the information provided by the artificial sensors from a hand prosthesis, physiologically appropriate (near-natural) sensory information can be provided to an amputee during the real-time decoding of different grasping tasks to control a dexterous hand prosthesis. This feedback enabled the participant to effectively modulate the grasping force of the prosthesis with no visual or auditory feedback. Three different force levels were distinguished and consistently used by the subject. The results also demonstrate that a high complexity of perception can be obtained, allowing the subject to identify the stiffness and shape of three different objects by exploiting different characteristics of the elicited sensations. This approach could improve the efficacy and “life-like” quality of hand prostheses, resulting in a keystone strategy for the near-natural replacement of missing hands.

Design of a cybernetic hand for perception and action

Strong motivation for developing new prosthetic hand devices is provided by the fact that low functionality and controllability—in addition to poor cosmetic appearance—are the most important reasons why amputees do not regularly use their prosthetic hands. This paper presents the design of the CyberHand, a cybernetic anthropomorphic hand intended to provide amputees with functional hand replacement. Its design was bio-inspired in terms of its modular architecture, its physical appearance, kinematics, sensorization, and actuation, and its multilevel control system. Its underactuated mechanisms allow separate control of each digit as well as thumb–finger opposition and, accordingly, can generate a multitude of grasps. Its sensory system was designed to provide proprioceptive information as well as to emulate fundamental functional properties of human tactile mechanoreceptors of specific importance for grasp-and-hold tasks. The CyberHand control system presumes just a few efferent and afferent channels and was divided in two main layers: a high-level control that interprets the user’s intention (grasp selection and required force level) and can provide pertinent sensory feedback and a low-level control responsible for actuating specific grasps and applying the desired total force by taking advantage of the intelligent mechanics. The grasps made available by the high-level controller include those fundamental for activities of daily living: cylindrical, spherical, tridigital (tripod), and lateral grasps. The modular and flexible design of the CyberHand makes it suitable for incremental development of sensorization, interfacing, and control strategies and, as such, it will be a useful tool not only for clinical research but also for addressing neuroscientific hypotheses regarding sensorimotor control.

Robotic techniques for upper limb evaluation and rehabilitation of stroke patients

This paper presents two robot devices for use in the rehabilitation of upper limb movements and reports the quantitative parameters obtained to characterize the rate of improvement, thus allowing a precise monitoring of patients recovery. A one degree of freedom (DoF) wrist manipulator and a two-DoF elbow-shoulder manipulator were designed using an admittance control strategy; if the patient could not move the handle, the devices completed the motor task. Two groups of chronic post-stroke patients (G1 n=7, and G2 n=9) were enrolled in a three week rehabilitation program including standard physical therapy (45 min daily) plus treatment by means of robot devices, respectively, for wrist and elbow-shoulder movements (40 min, twice daily). Both groups were evaluated by means of standard clinical assessment scales and a new robot measured evaluation metrics that included an active movement index quantifying the patients ability to execute the assigned motor task without robot assistance, the mean velocity, and a movement accuracy index measuring the distance of the executed path from the theoretic one. After treatment, both groups improved their motor deficit and disability. In G1, there was a significant change in the clinical scale values (p<0.05) and range of motion wrist extension (p<0.02). G2 showed a significant change in clinical scales (p<0.01), in strength (p<0.05) and in the robot measured parameters (p<0.01). The relationship between robot measured parameters and the clinical assessment scales showed a moderate and significant correlation (r>0.53 p<0.03). Our findings suggest that robot-aided neurorehabilitation may improve the motor outcome and disability of chronic post-stroke patients. The new robot measured parameters may provide useful information about the course of treatment and its effectiveness at discharge.

Double nerve intraneural interface implant on a human amputee for robotic hand control

OBJECTIVES The principle underlying this project is that, despite nervous reorganization following upper limb amputation, original pathways and CNS relays partially maintain their function and can be exploited for interfacing prostheses. Aim of this study is to evaluate a novel peripheral intraneural multielectrode for multi-movement prosthesis control and for sensory feed-back, while assessing cortical reorganization following the re-acquired stream of data. METHODS Four intrafascicular longitudinal flexible multielectrodes (tf-LIFE4) were implanted in the median and ulnar nerves of an amputee; they reliably recorded output signals for 4 weeks. Artificial intelligence classifiers were used off-line to analyse LIFE signals recorded during three distinct hand movements under voluntary order. RESULTS Real-time control of motor output was achieved for the three actions. When applied off-line artificial intelligence reached >85% real-time correct classification of trials. Moreover, different types of current stimulation were determined to allow reproducible and localized hand/fingers sensations. Cortical organization was observed via TMS in parallel with partial resolution of symptoms due to the phantom-limb syndrome (PLS). CONCLUSIONS tf-LIFE4s recorded output signals in human nerves for 4 weeks, though the efficacy of sensory stimulation decayed after 10 days. Recording from a number of fibres permitted a high percentage of distinct actions to be classified correctly. Reversal of plastic changes and alleviation of PLS represent corollary findings of potential therapeutic benefit. SIGNIFICANCE This study represents a breakthrough in robotic hand use in amputees.

Control of Hand Prostheses Using Peripheral Information

Several efforts have been carried out to enhance dexterous hand prosthesis control by impaired individuals. Choosing which voluntary signal to use for control purposes is a critical element to achieve this goal. This review presents and discusses the recent results achieved by using electromyographic signals, recorded either with surface (sEMG) or intramuscular (iEMG) electrodes, and electroneurographic (ENG) signals. The potential benefits and shortcomings of the different approaches are described with a particular attention to the definition of all the steps required to achieve an effective hand prosthesis control in the different cases. Finally, a possible roadmap in the field is also presented.

Towards a force-controlled microgripper for assembling biomedical microdevices

This paper presents recent results on the development and control of a microgripper based on flexure joints, fabricated by LIGA and instrumented with semiconductor strain-gauge force sensors. The microgripper is the end-effector of a workstation developed to grasp and manipulate tiny objects such as the components of a typical biomedical microdevice. The development of the force control in the microgripper is of fundamental importance in order to achieve the dexterity and sensing capabilities required to perform assembly tasks for biomedical microdevices. As a step towards the definition of the force control strategy, system identification techniques have been used to model the microgripper. Results indicate that a proportional integral (PI) controller could be used to assure, at the same time, closed-loop stability of the system, and a bandwidth suitable for the intended applications. The force control is based on strain-gauge sensors which have been integrated in the microgripper and experimentally characterized. Sensor response in the idling condition and during grasp showed that they can provide useful information for force control of the microgripper.

Assessing Mechanisms of Recovery During Robot-Aided Neurorehabilitation of the Upper Limb

Objective. The present study aimed to qualify and quantify the different components of motor recovery in a group of stroke patients treated by robot-aided techniques. In addition, the learning model of each motor recovery component was analyzed. Methods . Two groups of poststroke patients were treated with the use of an elbow-shoulder manipulator, respectively, within (recent) and after (chronic) the first 6 months of their cerebrovascular accident. Both groups were evaluated by means of standard clinical assessment scales and a robot-measured evaluation method. Results. These findings confirm that motor training consisting of voluntary movements assisted by the robot device led to significant improvements in motor performance in terms of the kinematic and dynamic components of the arm movements. This corresponded to improvement of impairment as confirmed by the clinical scale results. Conclusions. Knowledge of the recovery components and of the associated performance acquisition model may be useful in assessing and training stroke patients and should make it possible to precisely plan and, if necessary, modify the rehabilitation strategies.

A brain–spine interface alleviating gait deficits after spinal cord injury in primates

Spinal cord injury disrupts the communication between the brain and the spinal circuits that orchestrate movement. To bypass the lesion, brain–computer interfaces have directly linked cortical activity to electrical stimulation of muscles, and have thus restored grasping abilities after hand paralysis. Theoretically, this strategy could also restore control over leg muscle activity for walking. However, replicating the complex sequence of individual muscle activation patterns underlying natural and adaptive locomotor movements poses formidable conceptual and technological challenges. Recently, it was shown in rats that epidural electrical stimulation of the lumbar spinal cord can reproduce the natural activation of synergistic muscle groups producing locomotion. Here we interface leg motor cortex activity with epidural electrical stimulation protocols to establish a brain–spine interface that alleviated gait deficits after a spinal cord injury in non-human primates. Rhesus monkeys (Macaca mulatta) were implanted with an intracortical microelectrode array in the leg area of the motor cortex and with a spinal cord stimulation system composed of a spatially selective epidural implant and a pulse generator with real-time triggering capabilities. We designed and implemented wireless control systems that linked online neural decoding of extension and flexion motor states with stimulation protocols promoting these movements. These systems allowed the monkeys to behave freely without any restrictions or constraining tethered electronics. After validation of the brain–spine interface in intact (uninjured) monkeys, we performed a unilateral corticospinal tract lesion at the thoracic level. As early as six days post-injury and without prior training of the monkeys, the brain–spine interface restored weight-bearing locomotion of the paralysed leg on a treadmill and overground. The implantable components integrated in the brain–spine interface have all been approved for investigational applications in similar human research, suggesting a practical translational pathway for proof-of-concept studies in people with spinal cord injury.