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Novel Targeted Sensory Reinnervation Technique to Restore Functional Hand Sensation After Transhumeral Amputation Jacqueline S. Hebert, Jaret L. Olson, Michael J. Morhart, Michael R. Dawson, Paul D. Marasco, Todd A. Kuiken, and K. Ming Chan

Abstract—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. Index Terms—Electrical stimulation, myoelectric prosthesis, sensory feedback, tactile sensors, targeted reinnervation, upper limb amputation.

I. INTRODUCTION

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HE HUMAN hand is an exquisite sensory instrument that we regularly use to explore our surroundings by detecting minute details in objects, or guiding gracious movements such as those performed by pianists and surgeons. Indeed, as pointed out by John Napier, the hand is our eye that can “see” around the corner and in the dark [1]. Somatosensory inputs are vital components of motor performance executed by the upper limbs

Manuscript received August 22, 2013; revised November 08, 2013; accepted November 24, 2013. Date of publication December 18, 2013; date of current version July 03, 2014. J. S. Hebert and K. M. Chan are with the Division of Physical Medicine and Rehabilitation, Faculty of Medicine, University of Alberta, Edmonton, AB, T6R 2E1 Canada. J. L. Olson and M. J. Morhart are with the Department of Surgery, University of Alberta, Edmonton, AB, T6R 2E1 Canada. M. R. Dawson is with Glenrose Rehabilitation Hospital, Alberta Health Services, Edmonton, AB, T5G 0B7 Canada. P. D. Marasco is with the Department of Biomedical Engineering, Cleveland Clinic, Cleveland, OH 44195 USA. T. A. Kuiken is with the Center for Bionic Medicine, Rehabilitation Institute of Chicago, Chicago, IL 60611 USA. Color versions of one or more of the figures in this paper are available online at http://ieeexplore.ieee.org. Digital Object Identifier 10.1109/TNSRE.2013.2294907

[2]–[4]. In particular, the fingertips rely heavily on tactile afferents for sensory information to distinguish the object shape, mass, mass distribution, and friction of grasp necessary for fine motor control [4], [5]. Therefore, not surprisingly, traumatic amputation of the arm results in significant functional loss, and prosthetic replacement of dexterous hand function remains a challenge. Dexterous hand function requires multi-articulated grip patterns and sensory feedback, both of which have been identified by prosthetic users as high priority to improve prosthetic usage and acceptance [6]–[9]. With advancements in design of new multi-articular prosthetic limbs capable of multiple grip patterns and up to 22 degrees-of-freedom with embedded sensor technology [10], [11], the capacity of prosthetic limbs is starting to approach that of a human arm. The challenge lies in the development of a suitable human–machine interface to allow precise motor control and to receive and decode sensory information from the device. To address these issues, new techniques are being developed. Targeted muscle reinnervation is a surgical procedure for upper limb amputation that increases the number of intuitive outputs for myoelectric control. With this technique the amputated residual peripheral nerves are rerouted to remaining muscles in the residual limb [12]–[14]. The reinnervated target muscles provide natural physiologic motor commands to simultaneously control motions of the prosthetic limb [8], [15]–[18]. With improved motor control, the second issue of restoring sensory feedback from the prosthetic hand becomes a priority to enhance use of the prosthesis for fine dexterous tasks. In the past, various sensory substitution methods to provide feedback from a prosthesis have been attempted [19], [20] but have generally been unsuccessful in translation to clinical practice. This is likely due to lack of matching of the stimulus to physiologically natural or relevant sensations, as equivalency of association is a key requirement for useful prosthetic sensory feedback [21]. A practical method needs to be developed in which natural hand sensation can be elicited in the amputee, and linked to the action of the prosthetic device in order to provide intuitive feedback in a closed loop fashion. An exciting development in the quest for sensory restoration was discovered when the first patients who had undergone the targeted muscle reinnervation surgery were found to have restored hand sensations in the cutaneous area overlying the reinnervated muscles [16], [22]. This occurred in the initial sub-

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ject that had thinning of the subcutaneous tissue overlying the muscle sites, allowing sensory afferents from the main nerve trunks to competitively reinnervate the denervated skin [22]. An advancement in this technique was performed in subsequent subjects, who had deliberate denervation of cutaneous nerve branches, with end-to-side coaptation to the reinnervating main nerve trunks [16]. Several modalities of cutaneous sensation were restored in these subjects including touch, temperature, pain, and vibration with close to normal thresholds of perception [22]–[25], suggesting the regeneration of large mechanoreceptors as well as small diameter temperature and pain afferents. The prospect of using an area of reinnervated skin that carries near normal hand sensation to provide a meaningful sensory link to the prosthetic hand is tantalizing. Preliminary studies in targeted reinnervation subjects exploring the use of these cutaneous areas for sensory feedback with actuator devices show promising potential [26]. Limitations primarily relate to difficulties using skin areas overlying contractile muscle sites, and variable somatotopy of the hand map. To build on the earlier successes and with these limitations in mind, we developed a deliberate approach to specifically address critical requirements to make the deployment of the hand sensory map more practical for prosthetic application. In this paper, we describe a novel surgical addition to the targeted reinnervation procedure to increase control over the regenerating sensory nerve fibers from the median and ulnar nerves by targeting specific sensory cutaneous areas that do not overlie the reinnervated biceps and triceps muscles. This allows the incorporation of sensory feedback actuators over a separate territory without interference of the motor control sites. With this case we are able to demonstrate, for the first time, how the restored sensory hand maps can be used simultaneously with reinnervated muscle control for integrated sensory motor grip tasks. II. METHODS Using information from previous cadaver dissections as an anatomic map, we executed a novel targeted sensory reinnervation technique on a 20-year-old right handed man with left transhumeral amputation who sustained the injury through an industrial accident 10 months prior. The surgical plan for the procedure was to isolate fascicles of the median and ulnar nerves that carried high sensory content to coapt to specific target cutaneous nerves on the residual limb that would not overlie the muscle sites. We chose the median and ulnar nerves due to the high potential functional relevance of restoring palmar digit sensation. We used the standard targeted muscle reinnervation approach for transhumeral amputation as described by Dumanian et al. [14]. In addition to the identification of main nerve trunks and target motor branches, during the dissection we also identified the intercostobrachial cutaneous and axillary cutaneous nerve branches. Once the median nerve trunk was identified, we were able to isolate several fascicles of the median nerve through intrafascicular dissection [Fig. 1(a)]. To ensure that the fascicles chosen for sensory reinnervation had high sensory nerve fiber content, somatosensory evoked potentials (SSEP) on individual fascicles were performed using a 32 channel intraoperative monitoring system (Cascade, Cadwell Laboratory Inc, WA, USA). Silver chloride plated disk recording electrodes were placed on

the skull on a grid based on the international 10–20 system. For each stimulation the signals from the contralateral C4 (over the “hand” area of the post-central gyrus)-Cz montage were averaged from 60 stimuli provided at 3 Hz. Initially, the entire median nerve trunk was stimulated supramaximally to determine the maximum SSEP amplitude. Through intrafascicular dissection, individual fascicles were then lifted away from the nerve trunk and stimulated with a pair of silverball hook electrodes [Fig. 1(b)]. The individual fascicles stimulated showed wide ranges of SSEP amplitudes. The median fascicle showing the largest SSEP [fascicle trace shown in Fig. 1(c)] was chosen and further dissected out from the remainder of the nerve trunk, transected at the distal end and directly coapted in an end-to-end manner to the interocostobrachial cutaneous nerve (T2) close to its entry to the skin [Fig. 1(d)]. Then the remainder of the main trunk of the median nerve was coapted to the branch of the musculocutaneous nerve innervating the short head of the biceps muscle. A similar intrafascicular dissection and SSEP procedure was done on the ulnar nerve, and the selected sensory fascicle was dissected out for sufficient length to be coapted to the cutaneous branch of the axillary nerve close to its entry point to the skin [Fig. 1(d)]. The remainder of the main trunk of the ulnar nerve was then used to innervate the brachialis muscle. In the extensor compartment, only the motor procedure was performed with the distal portion of the radial nerve coapted to the motor branch of long head of the triceps muscle. A. Physiological Measures At baseline prior to the targeted reinnervation surgery, sensibility of the skin for pressure, temperature and heat pain threshold were measured within the innervation territory. To confirm the location and size of the denervated skin territory, the subject was examined at six weeks postoperation when the skin was insensate, using a 10 g monofilament to demarcate the boundary. The skin pressure sensitivity and anatomic sensory mapping were repeated at 4, 6, and 15 months post-surgery. At each assessment, a grid system with 2-D coordinates was superimposed over the skin of the residual limb. The points of stimulation were spaced 1 cm apart. Initially, a general assessment to map out areas of hand and digit sensations was performed using a cotton ball tip. To determine sensory threshold, Semmes-Weinstein Monofilaments were used to the lowest detectable threshold [27]. To determine discreteness of the digit sensations, a 2 g monofilament was used. To test reliability and consistency, each point on the grid was checked three times in random order and the subject was blindfolded to remove any visual cues. B. Performance Tasks To test functional outcomes of the novel targeted sensory reinnervation procedure, the subject was asked to perform a series of tasks using a robotic myoelectric training tool, shown in Fig. 2, at 15 months post-surgery. At the time of the performance testing, the subject was a daily user of his myoelectric prosthesis using two reinnervated and two native muscle sites in his transhumeral limb. The myoelectric training tool includes a robotic arm with an elbow, 2 degree-of-freedom wrist and a gripper that mimics the hand open/close movements of commercial prostheses by linearly mapping electromyography (EMG)

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Fig. 1. Inter-operative findings. A: Intrafascicular dissection of the median nerve after the epineurial sheath had been opened longitudinally. B: A pair of silverball electrodes was used to stimulate individual fascicles lifted away from the nerve trunk. C: Inter-operative SSEP recordings from the entire median nerve trunk (top three traces) and from stimulation of an individual fascicle. The fascicle that produced the largest SSEP was used for targeted sensory reinnervation. D: A summary schematic showing a fascicle of the median nerve (blue) was coapted to the intercostobrachial cutaneous (T2) nerve while a fascicle of the ulnar nerve (red) was connected to the cutaneous branch of the axillary nerve.

Fig. 2. Experimental setup of the myoelectric training tool that includes the AX-12 Smart Arm (Crustcrawler, Gilbert, AZ, USA) and a robotic gripper with two FSRs embedded at the tip. Subject controlled the myoelectric training tool relying exclusively on sensory feedback from the tactor while blind folded and with the sound of the motors blanked out by white noise.

signals to robotic joint velocities [28]. The elbow joint was controlled by electromyography (EMG) signals from the lateral biceps for flexion and medial triceps for extension. Opening and closing of the gripper was controlled by the EMG signals generated by the distal radial nerve reinnervated lateral triceps muscle and the median nerve reinnervated medial biceps muscle respectively. The robotic gripping device was capable of exerting up to 4 N of force. Two 0.5 force sensitive resistors (Solarbotics, Calgary, AB, Canada) were bonded to each tip of the gripping device adjacent to each other to measure grip pressure in two locations. To convey touch and pressure sensory feedback to the reinnervated skin, a HS-35HD servomotor actuator (Hitec RCD, Poway, CA, USA) connected to a rack and pinion mechanism (tactile stimulator or tactor) was secured to the skin in the intercostobrachial cutaneous nerve territory that carried sensation of the tip of the index finger (Fig. 2). A second tactor was secured to the axillary nerve territory that carried sensation for the fifth digit. The voltage output of each force sensitive resistor (FSR) was linked to the movement of each servomotor using a linear mapping. The movement limits of the servomotor were calibrated such that when there was no pressure on the FSR, the

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Fig. 3. Transfer sensation for the median nerve territory, mapped on transhumeral residual limb at 15 months post-operatively. The dots are 1 cm apart except those close to the end of the residual limb are slightly tapered. Discrete sensation in individual digits was abundant and spread over a wide area. Territory of the median nerve digits corresponded to the T2 intercostobrachial cutaneous nerve, measuring approximately 9 10 cm in surface area.

tactor head would be positioned far enough out of the skin to be below the subject’s detection threshold. When the maximum amount of pressure was sensed the tactor head would depress into the skin up to a depth of 2 cm, adjusted to the comfort and tolerance of the subject. After the EMG electrodes and sensory feedback tactors had been set up, the subject was given 10 min of practice operating the myoelectric training tool with sensory feedback to become familiar with the system by manipulating various objects. This practice time was unstructured, and included gripping and moving balls and foam blocks with varying sizes and consistencies, with the sensory feedback from the two tactors. During this time, qualitative comments were noted on the experienced sensations. Then a blindfold was applied to remove all visual cues and white noise delivered through a headset to remove any auditory clues while the subject performed a series of tasks. 1) Single Tactor Grip and Release Task: The subject was asked to grip, lift, and release a rubber ball using the myoelectric training tool. The task was solely guided by sensory feedback from a single tactor situated on the reinnervated skin carrying sensation of the index finger. To close the robotic gripper

Fig. 4. Transfer sensation for the ulnar nerve territory, mapped on transhumeral residual limb at 15 months post-operatively. Territory of the ulnar nerve hand map corresponded to the axillary nerve cutaneous distribution, measuring approximately 5 9 cm.

on the ball, the subject used volitional motor control from the surgically redirected median nerve to contract the reinnervated portion of the biceps muscle. As the gripper made initial contact with and firmly grasped the rubber ball, the subject was able to perceive those events through gradated feedback from the FSR to the tactor on his reinnervated skin. The subject lifted the ball by flexing the elbow joint of the myoelectric training tool controlled by the native innervated lateral biceps signal, and then released the rubber ball by contracting his reinnervated triceps muscle to open the gripper. The subject verbally reported perception of touch and pressure throughout the task. 2) Single Versus Dual Tactor Discrimination Task: This task utilized both sensory feedback systems, with one tactor attached to the median nerve distribution representing the index finger, and one to the ulnar nerve reinnervated fifth digit. The subject was presented with two foam blocks of identical consistency but different sizes. The small foam block contacted only one FSR on the robotic gripper, linked to median digit sensation, to represent a smaller object that would be expected to contact only the index finger. The larger foam block contacted both FSRs on the gripper, simulating a larger object that would be sensed by both the index and small finger. The subject was asked to report which size of block was presented to the gripper as he operated the gripper open/close function. The order of presentations

HEBERT et al.: NOVEL TARGETED SENSORY REINNERVATION TECHNIQUE TO RESTORE FUNCTIONAL HAND SENSATION

of the blocks was sequenced using a random number generator with blank presentations inserted to prevent random guessing. Three blocks of 10 presentations of each condition (small block, large block, and blank trial) giving 30 random presentations for each trial were administered and the results averaged across the three trials. 3) Force Discrimination Tasks: a) Force level detection: A tactor head attached to a FS03 force sensor (Honeywell, Morristown, NJ, USA) was applied to the reinnervated skin of the subject with two to five discrete levels of force including a “no-touch” condition in order to prevent random guessing. The forces applied to each territory were equally spaced between 0–3 N and 0–5 N for the median and ulnar territories respectively with the maximum forces limited according to the comfort of the subject. The discrete forces were randomly ordered and displayed with eight trials per force per number of levels. For each trial the subject was asked to verbally report which force they felt using a previously determined set of responses. For example, for two levels the responses were “no-touch” and “touch” and for three levels the responses were “no-touch,” “low,” and “high.” Responses were noted and the overall accuracy for each number of levels was computed. b) Object stiffness discrimination: Using the myoelectric training tool, two identical sized rubber balls, measuring 4 cm in diameter but with different stiffness were presented in random order to the subject. The harder ball had a stiffness of 750 N/m whereas the stiffness of the softer one was 235 N/m. The subject was asked to squeeze the presented ball with the gripper, and to indicate which ball was presented. As in the previous test, blanks were inserted to the test sequence to prevent random guessing. Three trials of 10 randomized presentations of each condition (soft ball, hard ball, and blank) were carried out and the results averaged. All functional performance data are reported using descriptive statistics as mean standard deviation (SD). Informed consent was obtained from the subject and the protocol received Health Ethics Research Board approval through our university. III. RESULTS A. Physiological Measures Using the Semmes-Weinstein Monofilaments at baseline preoperatively, we found uniform sensitivity of 0.008 g throughout the upper arm. Cold and warm thresholds as well as heat pain sensitivity were similar to that seen in the hand: cold threshold was at 6.8 just noticeable difference (JND) over the axillary cutaneous territory; it was 4.5 JND over the intercostobrachial nerve; and the threshold was 8.5 JND in the hand. Warm threshold was at 7.5 JND over both territories and 10.1 JND in the hand. Heat pain threshold was 20.3 over the axillary cutaneous territory and was 19.9 over the intercostobrachial nerve compared to 22.9 in the hand. The patient reported experiencing hand sensations at around three and a half months after surgery. At four months we did detailed sensory testing including pressure sensation and a percept map of the hand and digits. Compared to baseline, pressure sensitivity was much diminished in the cutaneously denervated territories, with a threshold of 6 g monofilament. In con-

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trast, skin sensitivity outside these territories in the upper arm remained the same. General mapping of hand and digit sensation was performed using a fine cotton ball tip. The digit sensations all fell within the boundaries of the recipient cutaneous nerves but with diminished sensibility. Also, the digits felt were in correspondence with the donor nerves used. In other words, the median nerve digit sensation corresponded with the intercostobrachial cutaneous nerve territory whereas the ulnar nerve innervated sensation corresponded with the axillary cutaneous nerve branch territory. We also compared temperature and pain thresholds at four months. In correspondence with the marked reduction in pressure sensitivity, sensitivity of the small sensory nerve fibers was also impaired. Cold thresholds were over 17.1 JND whereas warm thresholds had increased to above 18.6 JND. The subject reported gradual improvement in sensitivity over the ensuing months. The hand percept mapping was repeated at 15 months. Compared to the earlier time points, topographic representation of the digital sensations became more widely spread with multiple locations for each digit (Figs. 3 and 4). Compared to the fourth month postoperative sensory map, pressure sensitivity threshold had improved to 0.4 g monofilament. Subjectively, the subject reported that in the areas where single digits were felt, it was a feeling of his digit being touched with increasing pressure when greater force was applied. In areas where the subject could feel two or three digits the sensation was reported as “brushing” in quality. B. Performance Tasks 1) Single Tactor Grip and Release Task: Using only sensory feedback from a single tactor linked to one FSR on the gripper and without auditory or visual feedback, the subject was able to report when the gripping device had just come into contact with the rubber ball and when the ball was gripped tightly, corresponding to the readings of the FSR as initial and maximum pressure. The subject was able to lift the ball and to volitionally drop it, accurately reporting the release event. He stated he felt as though the ball was being touched by his index finger, with increasing pressure as he squeezed. He had consistent performance over 10 trials; he was able to identify contact, squeeze the ball, lift the ball and drop it on command 10 out of 10 times with no accidental drops. The results of a representative experiment are shown in Video, Supplementary Content 1. 2) Single Versus Dual Tactor Discrimination Task: The subject was able to detect single or dual simultaneous tactor stimulation by identifying the smaller block, larger block, or no block presentation correctly 28 out of 30 trials for an overall average accuracy of 93 6%. The subject reported the larger block gave the feeling of the object contacting both his index and small finger simultaneously, compared to the smaller block contacting only the index finger. As the trial progressed, the accuracy improved from 90% in the first two sets of presentations to 100% in the last set of presentation and less time was needed to correctly identify the objects. The results of a typical test are shown in Video, Supplemental Content 2. 3) Force Discrimination Task: a) Force level detection: Discrimination accuracy was 100% for discriminating touch/no-touch (two levels of discrim-

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Fig. 5. Discrimination accuracy. Two to five levels of force were applied to representative areas in the median (ventral index) and ulnar (dorsal fifth digit) reinnervated areas.

ination) in both territories. For three levels of force there was 100% accuracy in the fifth digit skin area and 88% for the index finger region. The force discrimination remained fairly accurate in the index finger region for four or five levels of force, staying above 80%, but for the fifth digit skin area accuracy decreased sharply past three levels of force (Fig. 5). b) Object stiffness discrimination: Using the tactor over the median innervated digit, the subject was able to discriminate between the hard ball, the soft ball or no ball in all 30 out of 30 presentations; he was correct 100% of the time. He was able to repetitively squeeze while sensing the resistance of each ball through graded pressure feedback from the tactor. A typical example is shown in Video, Supplemental Content 3. IV. DISCUSSION In this study, we demonstrate the feasibility of re-establishing separate median and ulnar sensory maps of the hand after transhumeral amputation by transferring individual fascicles with high sensory content from the median and ulnar nerves to different target cutaneous nerves on the residual limb. In addition to creating two spatially separated wide spread areas with discrete sensation for individual digits in the two nerve territories, we were able to demonstrate potential functional relevance by having the subject utilize this sensory feedback to execute tasks while operating a myoelectric training tool, without having to rely on visual guidance or auditory cues. Although a proof of principle study, this is a promising next step in the quest to develop sensory-motor integrated prostheses for natural dexterous manipulation. A. Somatotopy The hand maps that were restored were in completely separated skin areas. The median nerve sensory fascicle redirection restored a sensory map in the intercostobrachial nerve territory that only involved median nerve digits (volar surface of thumb, index, middle digit) with no overlap of ulnar nerve territory or native arm sensation. There was wide spread representation of the digits and good discrimination for sharp sensation. The ulnar

hand map was similarly solely confined to the targeted axillary nerve territory. There was more apparent representation of the dorsal ulnar cutaneous distribution for sharp discrete touch, and diffuse sensation of the volar fifth digit. This discrete separation of the median and ulnar hand maps is a notable difference from the overlap of ulnar and median nerve territories observed in prior sensory reinnervation subjects [16], [22]. The tightly clustered topographic expression of sensation at multiple sites for both reinnervation territories are in keeping with the fact that sensory nerve fibers destined to contiguous parts of the hand are well bundled and segregated even in proximal nerve trunks in the upper arm [29], [30]. The presented fascicular technique potentially assists with maintaining tighter somatotopy of the reinnervated cutaneous area by isolating a single sensory fascicle, which is more likely to represent contiguous digits, rather than allowing competitive reinnervation of all the afferents in the main nerve trunk. The redirection of the sensory fascicle to allow coaptation to the cutaneous nerve close to the skin entry point may also decrease the chance of competitive reinnervation of the target sensory end organs from afferent axons from other nearby nerve trunks, thereby avoiding overlap of territories. The contiguous distribution of digital representation over a large area may be practically advantageous. In addition to making placement of the tactor easier, minor displacement of the tactor on the skin during activities may not disrupt sensory feedback to the anatomically appropriate regions of the hand. Additionally, the widespread distribution of each digit would enable the mounting and use of multiple tactors. These tactors could target different digits in the median distribution or convey different sensory modalities from the same part of the prosthetic hand to different areas on the reinnervated skin. This would be important to overcome the noted limitation of poorer performance when multiple haptic sensations are applied to one reinnervated skin area [26], as different areas of the sensory map could potentially be used for different haptic modalities. B. The “Real Estate” Issue One of the challenges of restoring both motor output and sensory input access points on the residual limb is limited space. With the original targeted muscle reinnervation procedure, the sensory reinnervation tends to overlie the muscle sites, which can lead to difficulties when trying to implement all of the necessary hardware into the socket including EMG electrodes and sensory feedback devices in the same area. Furthermore, the muscle contraction itself can cause movement of the overlying skin. This was demonstrated with a haptic sensory feedback trial performed on subjects with the earlier reinnervation techniques, as subjects had difficulty simultaneously contracting their muscle for control and sensing the touch feedback [26]. This “real estate” problem is mitigated with the new proposed surgical technique, as the sensory fascicles are directed to cutaneous territories distant from the expected muscle electrode sites. This was confirmed by our subject’s ability to use his reinnervated and native innervated muscle sites to control the robotic arm, while simultaneously feeling the touch and pressure feedback in both sensory areas. Our approach using intrafascicular dissection allows a long

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recipient sensory fascicle to be isolated from the main nerve trunk and directed to a sensory cutaneous nerve that may be some distance from the intended motor reinnervation course of the main nerve. This is most obvious with the ulnar nerve redirection, where the single sensory fascicle was redirected from the medial arm to reach the target axillary cutaneous nerve on the lateral posterior aspect of the arm, as close to the skin entry point as possible. C. Sensory Discrimination The reinnervated territories recovered near normal thresholds for touch and temperature. This is consistent with prior targeted reinnervation subjects that have shown restored sensibility across many percepts, with close to normal thresholds of sensibility [16], [22], [23], [25]. In addition, the subject was able to sense force gradation quite sensitively. The subject did very well identifying up to three levels of force, even with our basic tactor set up. We were surprised at his accuracy in identifying ball stiffness, which implies that he was able to detect changes in force over a short amount of time. Our subject was able to discretely and simultaneously perceive touch from two separate tactors, matched to the hand maps representing touch on his index and little finger, and use this information in an identification task. This discrete digit sensation could potentially be linked to the fingers of a prosthetic device to provide somatotopically matched feedback. To our knowledge, this is the first time more than one tactor and sensory channel has been used with targeted reinnervation subjects. A recent study in subjects without targeted reinnervation evaluated the ability for spatial discrimination of sensors embedded in different digits of the prosthetic hand in transradial amputees. They found that those amputees with distinct referred phantom sensation of the digits had substantially better spatial discrimination compared to those without clear phantom sensation [31]. This finding is consistent with the high level spatial and force discrimination performance seen in our subject, and is important work in demonstrating the potential spatial resolution on the residual limb. However, those subjects were not required to use simultaneous motor control and were able to focus solely on the stimulation initiated by the investigator. The distinguishing feature for our subject was that he was able to sense touch to one or two digit areas simultaneous to motor control output, and use this information to reliably determine the size of the block placed in the gripper. An important advantage of targeted sensory reinnervation is that it enables the use of both anatomically and modality matched feedback. Haptic studies on prior reinnervation subjects have shown that applying force and tactile feedback can improve control of motor tasks in virtual environments [26], [32]. Our study has demonstrated that the restored sensory channel can be used while performing motor tasks with a physical robotic arm, providing physiologically relevant sensory feedback in a manner that is modality matched. This is an important consideration over sensory substitution methods. Although various forms of sensory substitution have been tried over the last several decades [19], [20], [33] no one method has been proven to be successful in clinical deployment. This may

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be related to the increased cognitive processing required to integrate nonphysiologically matched sensations. The goal of our case study was to overcome this, and match the anatomic location (digit for digit) as well as the modality (touch and pressure). Interestingly, during the practice sessions, it was noted that although the gripper did not resemble the shape of a hand, the subject reported the sensation of touching the ball with his own hand was quite strong. We are therefore quite hopeful that the restored sensory hand maps will provide an opportunity to physiologically and somatotopically match sensory feedback from the device to the individual’s sensory percept in a manner acceptable to the subject. D. Limitations This is a single case study, and consistency of outcome may differ for other individuals based on anatomic variation. In particular, the course of the intercostobrachial cutaneous nerve is known to be variable [34], and for some individuals may not be as discretely separated from the motor sites as was observed in our subject. Individual assessment for planning the optimal surgical approach is always required, but the SSEP technique does add one more layer of control by allowing separate sensory and motor reinnervation planning. Future potential targeted fascicular sensory approaches for other levels of upper limb amputation will need to take into account anatomic variation and cutaneous territories as part of the preoperative planning and intra-operative approach. Other limitations of our case study include the fact that the tasks were performed in a laboratory with a robotic training tool, rather than performance tasks using an actual prosthesis. However, we do feel that task performance with a robotic device was an important step as a proof of concept, compared to earlier work with virtual reality environments, as it required similar control and interaction effects as using prosthetic components. The performance tasks could have been designed with more complexity, but the main goal was to demonstrate the separation of the sensory input from the motor control, and the ability to have dual flow of information (motor and sensory) on the residual limb simultaneously. V. CONCLUSION We present a refinement of the targeted sensory reinnervation technique that allows an additional layer of control over sensory restoration after upper limb amputation. The use of intraoperative SSEP and intrafascicular dissection allowed specific targeting of sensory fascicles and rerouting to target cutaneous nerves at a distance away from the anticipated motor sites in a transhumeral amputee. Our proof of principle study demonstrated the ability to have dual flow of information within the residual limb, with control of a robotic arm using motor sites while simultaneously sensing touch and force feedback from a robotic gripper in a physiologically correct manner. Although clinical deployment of a sensory integrated prosthetic device has remaining challenges, the presented surgical method addresses the first issue of restoring a usable access point to provide natural hand sensation after upper limb amputation. The ability to restore physiologically appropriate touch feedback to

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an amputee in a way that they “feel” their prosthetic fingers gripping an object in a natural manner would be a major advancement in prosthetic replacement. ACKNOWLEDGMENT The authors would like to thank F. Roy for intraoperative neurophysiological monitoring, M. Stobbe and J. Carey for consultation advice, and J. Wong, T. Lin, R. Zhou, and J. Satkunam for assistance with data collection and graphics. REFERENCES [1] J. R. Napier, Hands. New York: Pantheon, 1980. [2] D. F. Collins and A. Prochazka, “Movement illusions evoked by ensemble cutaneous input from the dorsum of the human hand,” J. Physiol. (London), vol. 496, no. 3, pp. 857–871, Nov. 1996. [3] P. Jenmalm, S. Dahlstedt, and R. S. Johansson, “Visual and tactile information about object-curvature control fingertip forces and grasp kinematics in human dexterous manipulation,” J. Neurophysiol., vol. 84, no. 6, pp. 2984–2997, Dec. 2000. [4] R. S. Johansson and G. Westling, “Signals in tactile afferents from the fingers eliciting adaptive motor-responses during precision grip,” Exp. Brain Res., vol. 66, no. 1, pp. 141–154, Mar. 1987. [5] R. L. Sainburg, M. F. Ghilardi, H. Poizner, and C. Ghez, “Control of limb dynamics in normal subjects and patients without proprioception,” J. Neurophysiol., vol. 73, no. 2, pp. 820–835, Feb. 1995. [6] T. W. Wright, A. D. Hagen, and M. B. Wood, “Prosthetic usage in major upper extremity amputations,” J. Hand Surg., vol. 20, no. 4, pp. 619–622, Jun. 1995. [7] D. J. Atkins, D. C. Heard, and W. H. Donovan, “Epidemiologic overview of individuals with upper-limb loss and their reported research priorities,” J. Prosth. Orthot., vol. 8, no. 1, pp. 2–8, Jun. 1996. [8] J. B. Hijjawi, T. A. Kuiken, R. D. Lipschutz, L. A. Miller, K. A. Stubblefield, and G. A. Dumanian, “Improved myoelectric prosthesis control accomplished using multiple nerve transfers,” Plast. Reconstr. Surg., vol. 118, no. 7, pp. 1573–1578, Dec. 2006. [9] E. Biddiss, D. Beaton, and T. Chau, “Consumer design priorities for upper limb prosthetics,” Disabil. Rehabil. Assist. Technol., vol. 2, no. 6, pp. 346–357, Jan. 2007. [10] A. Harris, K. Katyal, M. Para, and J. Thomas, “Revolutionizing Prosthetics software technology,” in Proc. IEEE Int. Conf. Syst., Man Cybern., 2011, pp. 2877–2884. [11] R. S. Armiger, F. V. Tenore, K. D. Katyal, M. S. Johannes, A. Makhlin, M. L. Natter, J. E. Colgate, S. J. Bensmaia, and R. J. Vogelstein, “Enabling closed-loop control of the modular prosthetic limb through haptic feedback,” Johns Hopkins APL Tech. Dig., vol. 31, no. 4, pp. 345–353, May 2013. [12] T. A. Kuiken, G. A. Dumanian, R. D. Lipschutz, L. A. Miller, and K. A. Stubblefield, “The use of targeted muscle reinnervation for improved myoelectric prosthesis control in a bilateral shoulder disarticulation amputee,” Pros. Ortho. Int., vol. 28, no. 3, pp. 245–253, May 2004. [13] K. D. O’Shaughnessy, G. A. Dumanian, R. D. Lipschutz, L. A. Mille, K. Stubblefield, and T. A. Kuiken, “Targeted reinnervation to improve prosthesis control in transhumeral amputees: A report of three cases,” J. Bone Joint Surg., vol. 90, no. 2, pp. 393–400, Feb. 2008. [14] G. A. Dumanian, J. H. Ko, K. D. O’Shaughnessy, P. S. Kim, C. J. Wilson, and T. A. Kuiken, “Targeted reinnervation for transhumeral amputees: Current surgical technique and update on results,” Plast. Reconstr. Surg., vol. 124, no. 3, pp. 863–869, Sep. 2009. [15] R. D. Lipschutz, T. A. Kuiken, L. A. Miller, G. A. Dumanian, and K. A. Stubblefield, “Shoulder disarticulation externally powered prosthetic fitting following targeted muscle reinnervation for improved myoelectric control,” J. Prosth. Orthot., vol. 18, no. 2, pp. 28–34, Jun. 2006. [16] T. A. Kuiken, R. D. Lipschutz, B. A. Lock, K. A. Stubblefield, P. D. Marasco, P. Zhou, and G. A. Dumanian, “Targeted reinnervation for enhanced prosthetic arm function in a woman with a proximal amputation: A case study,” Lancet, vol. 369, no. 9559, pp. 371–380, Jan. 2007.

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Jacqueline S. Hebert received the M.D. degree from the University of Calgary, Calgary, AB, Canada, in 1995, and the fellowship in physical medicine and rehabilitation at the University of Alberta, Edmonton, AB, Canada, in 2000. She is Associate Professor in the Division of Physical Medicine and Rehabilitation, Faculty of Medicine and Dentistry at the University of Alberta, Edmonton, AB, Canada, and the medical lead of the Adult Amputee Program at the Glenrose Rehabilitation Hospital, Edmonton, AB, Canada. In 2012, she was appointed Associate Research Chair in Clinical Rehabilitation with the Faculty of Rehabilitation Medicine.

HEBERT et al.: NOVEL TARGETED SENSORY REINNERVATION TECHNIQUE TO RESTORE FUNCTIONAL HAND SENSATION

Jaret L. Olson completed his fellowship in pediatric plastic surgery at The Hospital for Sick Children, Toronto, ON, Canada, in 2002. He is Associate Professor at the University of Alberta, plastic surgery pediatric lead, and one of the primary surgeons for the brachial plexus reconstruction clinic in Edmonton, AB, Canada. Dr. Olson is a member of the Royal College of Physicians and Surgeons of Canada Plastic Surgery National Examination Committee.

Michael J. Morhart completed the M.D. degree in 1994. He completed his plastic surgery training at the University of Alberta, Edmonton, AB, Canada, in 1999, and an orthopedic fellowship in hand, wrist and microsurgery at the University of Utah, Salt Lake City, UT, USA, in 2002. He is currently a Clinical Professor at the Department of Surgery, University of Alberta, Edmonton, AB, Canada.

Michael R. Dawson received the B.Sc. and M.Sc. degrees in mechanical engineering with research focus on developing a myoelectric training tool for upper-limb amputees from the University of Alberta, Edmonton, AB, Canada, in 2008 and 2011, respectively. He works as a Research Associate for the Glenrose Rehabilitation Hospital, Edmonton, AB, Canada, and assists in the development of machine learning controllers and sensory feedback systems.

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Paul D. Marasco received the Ph.D. degree in neuroscience from Vanderbilt University, Nashville, TN, USA. He is an Associate Staff Scientist in the Department of Biomedical Engineering in the Lerner Research Institute at Cleveland Clinic, Cleveland, OH, USA. He is a Research Health Scientist in the Advanced Platform Technology Center of Excellence and Director of Amputee Research for the Department of Physical Medicine and Rehabilitation at the Louis Stokes Cleveland Department of Veterans Affairs Medical Center, Cleveland, OH, USA. His research interests include sensory integration with prosthetics, sensory-neural brain organization and plasticity and cognitive approaches to restoration of function.

Todd A. Kuiken received the M.D. and Ph.D. degrees in biomedical engineering from Northwestern University, Chicago, IL, USA, in 1990, and completed his residency in physical medicine and rehabilitation at the Rehabilitation Institute of Chicago, Chicago, IL, USA, in 1995. He is currently is the Director of the Center for Bionic Medicine, Chicago, IL, USA. He is a Professor in the Departments of Physical Medicine and Rehabilitation, Biomedical Engineering, and Surgery at Northwestern University, Chicago, IL, USA.

K. Ming Chan received the MB, ChB from Glasgow University, Glasgow, U.K., in 1984. He completed residency training at the University of Alberta, Edmonton, AB, Canada, and fellowship training at Tufts University, Boston, MA, USA. He is a Professor in Physical Medicine and Rehabilitation with an adjunct appointment at the Centre for Neuroscience, University of Alberta, Edmonton, AB, Canada. His research interests are in peripheral nerve regeneration, myoelectric prosthetic control, and neurodegenerative disorders.