From the Cover: Neural interfacing architecture enables enhanced motor control and residual limb functionality postamputation

Despite advancements in prosthetic technologies, patients with amputation today suffer great diminution in mobility and quality of life. We have developed a modified below-knee amputation (BKA) procedure that incorporates agonist–antagonist myoneural interfaces (AMIs), which surgically preserve and couple agonist–antagonist muscle pairs for the subtalar and ankle joints. AMIs are designed to restore physiological neuromuscular dynamics, enable bidirectional neural signaling, and offer greater neuroprosthetic controllability compared to traditional amputation techniques. In this prospective, nonrandomized, unmasked study design, 15 subjects with AMI below-knee amputation (AB) were matched with 7 subjects who underwent a traditional below-knee amputation (TB). AB subjects demonstrated significantly greater control of their residual limb musculature, production of more differentiable efferent control signals, and greater precision of movement compared to TB subjects (P < 0.008). This may be due to the presence of greater proprioceptive inputs facilitated by the significantly higher fascicle strains resulting from coordinated muscle excursion in AB subjects (P < 0.05). AB subjects reported significantly greater phantom range of motion postamputation (AB: 12.47 ± 2.41, TB: 10.14 ± 1.45 degrees) when compared to TB subjects (P < 0.05). Furthermore, AB subjects also reported less pain (12.25 ± 5.37) than TB subjects (17.29 ± 10.22) and a significant reduction when compared to their preoperative baseline (P < 0.05). Compared with traditional amputation, the construction of AMIs during amputation confers the benefits of enhanced physiological neuromuscular dynamics, proprioception, and phantom limb perception. Subjects’ activation of the AMIs produces more differentiable electromyography (EMG) for myoelectric prosthesis control and demonstrates more positive clinical outcomes.

The standard-of-care surgical approach to amputation has not seen considerable innovation since its conception in the mid-1800s (1), despite significant progress in biomechatronics and advanced reconstructive techniques. The typical amputation procedure neglects neurological substrates and disrupts key neuromuscular relationships responsible for bidirectional (efferent, afferent) signaling. The deafferentation of lower motor neurons triggers central reorganization of motor circuits, which negatively impacts motor imagery and motor coordination (2, 3) and results in significant neuroma pain (4–6), phantom pain (7), and maladaptive or diminishing phantom sensation (8–10). Phantom sensation, the perception of one’s phantom limb while at rest and in motion, is an important component of motor imagery utilized in the preparation of motor control commands and can be a source of chronic irritation, if unpleasant. The haphazard arrangement and myodesis of residual musculature further constrain the ability for individual muscles to dynamically excurse, causing cocontraction of muscles and changing gait patterns (11–14). Together, these peripheral and central modifications result in the poor production of efferent signals for direct myoelectric control (15, 16). To compensate for these shortcomings, considerable effort has been spent on developing and deploying pattern-recognition–based myoelectric control strategies (17–19). However, even with these advanced myoelectric devices and controllers, end users find their operation cumbersome and time consuming (20). Motor control is also challenged by the lack of proprioceptive sensory feedback from prostheses (12, 21–23). Together, the limitations of the current amputation approaches significantly lower the quality of life for persons with amputation (24–27).In recognition of these shortcomings, surgical researchers have recently begun to explore new strategies to modify standard amputation procedures. Targeted muscle reinnervation (TMR) (28, 29) and regenerative peripheral nerve interfaces (RPNIs) (30, 31) represent approaches that are designed to provide greater efferent motor signals for myoelectric control and mitigate neuroma pain. However, neither approach offers muscle–tendon afferent proprioceptive signaling, which is physiologically mediated by agonist–antagonist muscle dynamics and critical for trajectory planning, fine motor control, and reflexes (32, 33).The agonist–antagonist myoneural interface (AMI) is a more recent surgical approach and neural interfacing strategy designed to augment volitional motor control and restore muscle–tendon proprioception (11, 12, 34–37) by surgically coapting agonist and antagonist muscles to restore natural physiological muscle pairing and dynamics. When the agonist muscle contracts, the antagonist muscle stretches (or vice versa), giving rise to musculotendinous afferent feedback from muscle spindle fibers (length and velocity) and Golgi tendon organs (force). For each joint in a bionic limb, one AMI is surgically constructed in the residuum. Functional electrical stimulation (FES) applied to the antagonist muscle of the AMI can provide force or position feedback onto the agonist (or vice versa) from a bionic prosthesis to inform the user of prosthetic torque or position, respectively (11). In Clites et al. (11), an early human subject with an AMI amputation demonstrated dynamic muscle excursions, individualized contraction of each AMI muscle, and graded proprioceptive muscle–tendon feedback in response to muscle activation. This subject additionally demonstrated greater control of joint position, impedance, and FES-based torque feedback from a bionic prosthesis when compared to subjects with a traditional amputation. This pilot study demonstrated the potential of the AMI and paved the way for further implementation and investigation of the physiological properties, phantom limb perceptions, pain, and motor control of the AMI neuromuscular constructs.In this study, we characterize the physiological outcomes of subjects with an AMI below-knee amputation (AB) (n = 15) and compare them against those of matched control subjects with a traditional below-knee amputation (TB) (n = 7). Given the emphasis placed on the reconstruction of peripheral neuromusculature with AMIs, we hypothesize that the AB cohort will experience an enhancement in phantom sensation and range of motion (ROM) percepts compared with the TB cohort. As a result of the dynamically coupled agonist–antagonist muscles comprising the AMI constructs, we also hypothesize that the AB cohort will demonstrate greater muscle excursion and fascicle strains compared to the TB population. With these improvements in residual limb muscle dynamics, motor capabilities, and perception, we further anticipate that AB subjects will demonstrate greater accuracy and precision of performance on ankle and subtalar intended movements compared to matched TB participants. These hypotheses are evaluated through a combination of electromyography (EMG), goniometry, ultrasonography, and surveys.