Paul D. Marasco

Novel targeted sensory reinnervation technique to restore functional hand sensation after transhumeral amputation.

We present a case study of a novel variation of the targeted sensory reinnervation technique that provides additional control over sensory restoration after transhumeral amputation. The use of intraoperative somatosensory evoked potentials on individual fascicles of the median and ulnar nerves allowed us to specifically target sensory fascicles to reroute to target cutaneous nerves at a distance away from anticipated motor sites in a transhumeral amputee. This resulted in restored hand maps of the median and ulnar nerve in discrete spatially separated areas. In addition, the subject was able to use native and reinnervated muscle sites to control a robotic arm while simultaneously sensing touch and force feedback from the robotic gripper in a physiologically correct manner. This proof of principle study is the first to demonstrate the ability to have simultaneous dual flow of information (motor and sensory) within the residual limb. In working towards clinical deployment of a sensory integrated prosthetic device, this surgical method addresses the important issue of restoring a usable access point to provide natural hand sensation after upper limb amputation.

The effect of biomechanical variables on force sensitive resistor error: Implications for calibration and improved accuracy.

Force Sensitive Resistors (FSRs) are commercially available thin film polymer sensors commonly employed in a multitude of biomechanical measurement environments. Reasons for such wide spread usage lie in the versatility, small profile, and low cost of these sensors. Yet FSRs have limitations. It is commonly accepted that temperature, curvature and biological tissue compliance may impact sensor conductance and resulting force readings. The effect of these variables and degree to which they interact has yet to be comprehensively investigated and quantified. This work systematically assesses varying levels of temperature, sensor curvature and surface compliance using a full factorial design-of-experiments approach. Three models of Interlink FSRs were evaluated. Calibration equations under 12 unique combinations of temperature, curvature and compliance were determined for each sensor. Root mean squared error, mean absolute error, and maximum error were quantified as measures of the impact these thermo/mechanical factors have on sensor performance. It was found that all three variables have the potential to affect FSR calibration curves. The FSR model and corresponding sensor geometry are sensitive to these three mechanical factors at varying levels. Experimental results suggest that reducing sensor error requires calibration of each sensor in an environment as close to its intended use as possible and if multiple FSRs are used in a system, they must be calibrated independently.

Illusory movement perception improves motor control for prosthetic hands

A perceptual illusion provides the sensation of complex bionic hand movements to human amputees, allowing real-time movement control without the necessity of vision. Good vibrations for movement perception The ability to sense the spatial position and movements of one’s own body (kinesthetic sense) is critical for limb use. Because prostheses do not provide physical feedback during movement, amputees may not feel that they are in control of their bodily movements (sense of agency) when manipulating a prosthesis. Marasco et al. developed an automated neural-machine interface that vibrates the muscles used for control of prosthetic hands. This system instilled kinesthetic sense in amputees, allowing them to control prosthetic hand movements in the absence of visual feedback and increasing their sense of agency. This approach might be an effective strategy for improving motor performance and quality of life in amputees. To effortlessly complete an intentional movement, the brain needs feedback from the body regarding the movement’s progress. This largely nonconscious kinesthetic sense helps the brain to learn relationships between motor commands and outcomes to correct movement errors. Prosthetic systems for restoring function have predominantly focused on controlling motorized joint movement. Without the kinesthetic sense, however, these devices do not become intuitively controllable. We report a method for endowing human amputees with a kinesthetic perception of dexterous robotic hands. Vibrating the muscles used for prosthetic control via a neural-machine interface produced the illusory perception of complex grip movements. Within minutes, three amputees integrated this kinesthetic feedback and improved movement control. Combining intent, kinesthesia, and vision instilled participants with a sense of agency over the robotic movements. This feedback approach for closed-loop control opens a pathway to seamless integration of minds and machines.

The neural response properties and cortical organization of a rapidly adapting muscle sensory group response that overlaps with the frequencies that elicit the kinesthetic illusion

Kinesthesia is the sense of limb movement. It is fundamental to efficient motor control, yet its neurophysiological components remain poorly understood. The contributions of primary muscle spindles and cutaneous afferents to the kinesthetic sense have been well studied; however, potential contributions from muscle sensory group responses that are different than the muscle spindles have not been ruled out. Electrophysiological recordings in peripheral nerves and brains of male Sprague Dawley rats with a degloved forelimb preparation provide evidence of a rapidly adapting muscle sensory group response that overlaps with vibratory inputs known to generate illusionary perceptions of limb movement in humans (kinesthetic illusion). This group was characteristically distinct from type Ia muscle spindle fibers, the receptor historically attributed to limb movement sensation, suggesting that type Ia muscle spindle fibers may not be the sole carrier of kinesthetic information. The sensory-neural structure of muscles is complex and there are a number of possible sources for this response group; with Golgi tendon organs being the most likely candidate. The rapidly adapting muscle sensory group response projected to proprioceptive brain regions, the rodent homolog of cortical area 3a and the second somatosensory area (S2), with similar adaption and frequency response profiles between the brain and peripheral nerves. Their representational organization was muscle-specific (myocentric) and magnified for proximal and multi-articulate limb joints. Projection to proprioceptive brain areas, myocentric representational magnification of muscles prone to movement error, overlap with illusionary vibrational input, and resonant frequencies of volitional motor unit contraction suggest that this group response may be involved with limb movement processing.

High-density peripheral nerve cuffs restore natural sensation to individuals with lower-limb amputations

OBJECTIVE Sensory input in lower-limb amputees is critically important to maintaining balance, preventing falls, negotiating uneven terrain, responding to unexpected perturbations, and developing the confidence required for societal participation and public interactions in unfamiliar environments. Despite noteworthy advances in robotic prostheses for lower-limb amputees, such as microprocessor knees and powered ankles, natural somatosensory feedback from the lost limb has not yet been incorporated in current prosthetic technologies. APPROACH In this work, we report eliciting somatic sensation with neural stimulation delivered by chronically-implanted, non-penetrating nerve cuff electrodes in two transtibial amputees. High-density, flexible, 16-contact nerve cuff electrodes were surgically implanted for the selective activation of sensory fascicles in the nerves of the posterior thigh above the knee. Electrical pulses at safe levels were delivered to the nerves by an external stimulator via percutaneous leads attached to the cuff electrodes. MAIN RESULTS The neural stimulation was perceived by participants as sensation originating from the missing limb. We quantitatively and qualitatively ascertained the intensity, modality as well as the location and stability of the perceived sensations. Stimulation through individual contacts within the nerve cuffs evoked repeatable sensations of various modalities and at discrete locations projected to the missing toes, foot and ankle, as well as in the residual limb. In addition, we observed a high overlap in reported locations between distal versus proximal cuffs suggesting that the same sensory responses could be elicited from more proximal points on the nerve. SIGNIFICANCE Based on these findings, the high-density cuff technology is suitable for restoring natural sensation to lower-limb amputees and could be utilized in developing a neuroprosthesis with natural sensory feedback. The overlap in reported locations between proximal and distal cuffs indicates that our approach might be applicable to transfemoral amputees where distal muscles and branches of sciatic nerve are not available.

Characterization of interfacial socket pressure in transhumeral prostheses: A case series

One of the most important factors in successful upper limb prostheses is the socket design. Sockets must be individually fabricated to arrive at a geometry that suits the user’s morphology and appropriately distributes the pressures associated with prosthetic use across the residual limb. In higher levels of amputation, such as transhumeral, this challenge is amplified as prosthetic weight and the physical demands placed on the residual limb are heightened. Yet, in the upper limb, socket fabrication is largely driven by heuristic practices. An analytical understanding of the interactions between the socket and residual limb is absent in literature. This work describes techniques, adapted from lower limb prosthetic research, to empirically characterize the pressure distribution occurring between the residual limb and well-fit transhumeral prosthetic sockets. A case series analyzing the result of four participants with transhumeral amputation is presented. A Tekscan VersaTek pressure measurement system and FaroArm Edge coordinate measurement machine were employed to capture socket-residual limb interface pressures and geometrically register these values to the anatomy of participants. Participants performed two static poses with their prosthesis under two separate loading conditions. Surface pressure maps were constructed from the data, highlighting pressure distribution patterns, anatomical locations bearing maximum pressure, and the relative pressure magnitudes. Pressure distribution patterns demonstrated unique characteristics across the four participants that could be traced to individual socket design considerations. This work presents a technique that implements commercially available tools to quantitatively characterize upper limb socket-residual limb interactions. This is a fundamental first step toward improved socket designs developed through informed, analytically-based design tools.

Artificial Limbs for Upper Extremity Amputation

The importance of integrating the surgical, prosthetic, and rehabilitation treatment of a person with upper limb loss to optimize outcome has never been more evident. A limb amputation leaves a number of critical structural challenges that can be optimized by diligent surgical approaches. Advances in socket technology, prosthetic components, and control strategies have improved dramatically over the last decade. Exciting developments in neural interface control, signal processing, and engineered devices create a shifting landscape of which surgeons and rehabilitation practitioners need to be aware in order to create optimal outcomes for patients with limb loss. This chapter provides an overview of the current state-of-the-art surgical and prosthetic management approaches for upper limb amputation, as well as a glance at some of the exciting developments on the horizon.

Using proprioception to get a better grasp on embodiment

We interact with, interpret and understand the world around us through our senses. We see our environment, touch the things in it, feel the ground beneath our feet, and know how we move within our surroundings. This rich multisensory information stream not only forms the basis of our impression of the world, but also establishes our intrinsic sense of self within that world. By integrating these sensory streams we perceptually separate ourselves from the environment around us: an ‘I’ among a world of ‘other’. For instance, when we see and feel a touch to our hand we know that hand is a part of our body and it belongs to us. When we see another person being touched, without feeling that same touch, we know that other body is not ours. Although we take for granted the simple and basic sense that our arms, legs and bodies belong to us, this innate perception of ownership or embodiment is much more malleable than we might ever have imagined. Humans have long reflected on the idea of the self, the sense that you observe the world from an internal perspective that is distinct from others and separate from the external (Reid, 2002). Until recently, investigation of the concept of self has been confined to the realm of philosophy. However, in 1998 Botvinick and Cohen demonstrated that through a simple manipulation of seen and felt touch, able-bodied individuals could be fooled into perceiving that a fake hand was their own hand (Botvinick & Cohen, 1998). This phenomenon of inducing cognitive embodiment of a hand that is not actually part of the body is known as the ‘rubber hand illusion’, and it is simple to generate. A participant is seated with his or her hands outstretched comfortably in front on a table top, with one hand hidden from view behind a screen. A rubber hand is positioned in place of the hidden hand in the same orientation and within the participant’s correct visual frame of reference. An experimenter sits across from the participant and simultaneously strokes the rubber hand (that the participant can see) and the participant’s hidden hand (that the participant cannot see) in the same way with the same timing. After a few seconds most participants will feel the experimenter’s touch as though it was occurring on the rubber hand; as though it was their own hand. During this transition the participant cognitively incorporates the fake hand into his or her self-image (Botvinick & Cohen, 1998), while simultaneously, disincorporating his or her actual hand (Newport & Preston, 2011). This embodiment illusion has opened the door to experimental approaches that are now beginning to tease apart the brain circuits and cognitive/perceptual mechanisms that underlie the sense of self (Blanke, 2012). In this issue of The Journal of Physiology, Héroux and colleagues (2018) present their work providing insight into the mechanisms of self-attribution. Using their ‘grasp illusion’, a new variant of the rubber hand illusion, this team separated out individual components of the sensory streams to explore how the brain integrates information about relevant features to generate the sense of embodiment. The grasp illusion arises when a participant, who cannot see his or her hands, grasps a hidden fake finger positioned such that it appears to be in the same orientation as his or her other actual finger. Simultaneously, the tip of the participant’s actual finger, which is sitting at a distance directly below the fake finger, is lightly clamped so as to feel as though it is being grasped. When this is done, the participant perceives that his or her two hands are aligned more closely in vertical space than they actually are. In this study, Héroux and colleagues found that the perception that the fingers are more closely aligned occurs very rapidly after the proprioceptive input from the grasp, and that a reported sense of ownership over the fake finger also occurred at the initial grasp and grew stronger over the 3 min of the experiment. This is interesting because it suggests that body ownership is not necessarily tied solely to vision and touch, and that the brain likely uses relevant sensory inputs such as proprioceptive position sense from the skin to generate a feeling of self-attribution. The authors also investigate the influence of physical characteristics of fake fingers on ownership and perceived location. Participants grasped fake fingers that were hot or cold, pliable or hard, rough or smooth, and rectangular or oddly shaped. The characteristics of the fake finger did have an effect on the sense of embodiment and perceived alignment in vertical space even though the fake finger was never actually seen during the experiments. It just happened to be ‘like’ a finger, and perceived as if it were a finger. Most interestingly, grasping a cold finger, a rough finger, or an oddly shaped or rectangular finger all reduced embodiment. This is a particularly compelling finding because it suggests that the brain has an innate representation or pre-supposition of what a finger should feel like. Thus the sensory integration system likely weights levels of embodiment within the context of physical relevance. This is important because there is debate as to how flexible our sense of ownership is and this study provides evidence that in order to be incorporated into the self-image, the fake body part should feel, at least nominally, like an actual body part (Hohwy & Paton, 2010). In addition to exploring new methods for understanding embodiment, Héroux and colleagues also stepped outside of the traditional P-value approach for interpreting data. Human perception is complex and restricting analyses to results of yes or no risks missing underlying nuances of experience. The authors achieved an unprecedented level of transparency by presenting individual participant data overlaid with the summaries and by providing raw data and their analysis code in an online repository.

Fitts’ Law in the Control of Isometric Grip Force With Naturalistic Targets

Fitts’ law models the relationship between amplitude, precision, and speed of rapid movements. It is widely used to quantify performance in pointing tasks, study human-computer interaction, and generally to understand perceptual-motor information processes, including research to model performance in isometric force production tasks. Applying Fitts’ law to an isometric grip force task would allow for quantifying grasp performance in rehabilitative medicine and may aid research on prosthetic control and design. We examined whether Fitts’ law would hold when participants attempted to accurately produce their intended force output while grasping a manipulandum when presented with images of various everyday objects (we termed this the implicit task). Although our main interest was the implicit task, to benchmark it and establish validity, we examined performance against a more standard visual feedback condition via a digital force-feedback meter on a video monitor (explicit task). Next, we progressed from visual force feedback with force meter targets to the same targets without visual force feedback (operating largely on feedforward control with tactile feedback). This provided an opportunity to see if Fitts’ law would hold without vision, and allowed us to progress toward the more naturalistic implicit task (which does not include visual feedback). Finally, we changed the nature of the targets from requiring explicit force values presented as arrows on a force-feedback meter (explicit targets) to the more naturalistic and intuitive target forces implied by images of objects (implicit targets). With visual force feedback the relation between task difficulty and the time to produce the target grip force was predicted by Fitts’ law (average r2 = 0.82). Without vision, average grip force scaled accurately although force variability was insensitive to the target presented. In contrast, images of everyday objects generated more reliable grip forces without the visualized force meter. In sum, population means were well-described by Fitts’ law for explicit targets with vision (r2 = 0.96) and implicit targets (r2 = 0.89), but not as well-described for explicit targets without vision (r2 = 0.54). Implicit targets should provide a realistic see-object-squeeze-object test using Fitts’ law to quantify the relative speed-accuracy relationship of any given grasper.

Setting the pace: insights and advancements gained while preparing for an FES bike race

The reduction in physical activity following a spinal cord injury often leads to a decline in mental and physical health. Developing an exercise program that is effective and enjoyable is paramount for this population. Although functional electrical stimulation (FES) stationary cycling has been utilized in rehabilitation settings, implementing an overground cycling program for those with spinal cord injuries has greater technical challenges. Recently our laboratory team focused on training five individuals with compete spinal cord injuries utilizing an implanted pulse generator for an overground FES bike race in CYBATHLON 2016 held in Zurich, Switzerland. The advancements in muscle strength and endurance and ultimately cycling power our pilots made during this training period not only helped propel our competing pilot to win gold at the CYBATHLON 2016, but allowed our pilots to ride their bikes outside within their communities. Such a positive outcome has encouraged us to put effort into developing more widespread use of FES overground cycling as a rehabilitative tool for those with spinal cord injuries. This commentary will describe our approach to the CYBATHLON 2016 including technological advancements, bike design and the training program.