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There is growing evidence on the efficacy of electrical stimulation delivered via spinal neural interfaces to improve functional recovery following spinal cord injury. For such interfaces, carbon-based neural arrays are fast becoming recognized as a compelling material and platform due to biocompatibility and long-term electrochemical stability. Here, we introduce the design, fabrication, and in vivo characterization of a novel cervical epidural implant with carbon-based surface electrodes. Through finite element analysis and mechanical load tests, we demonstrated that the array could safely withstand loads applied to it during implantation and natural movement of the subject with minimal stress levels. Furthermore, the long-term in vivo performance of this neural array consisting of glassy carbon surface electrodes was investigated through acute and chronic spinal motor evoked potential recordings and electrode impedance tests in rats. We demonstrated stable stimulation performance for at least four weeks in a rat model of spinal cord injury. Lastly, we found that impedance measurements on all carbon-based spinal arrays were generally stable over time up to four weeks after implantation, with a slight increase in impedance in subsequent weeks when tested in spinally injured rats. Taken together, this study demonstrated the potential for carbon-based electrodes as a spinal neural interface to accelerate both mechanistic research and functional restoration in animal models of spinal cord injury.

Paralysis of the upper extremity severely restricts independence and quality of life after spinal cord injury. Regaining control of hand and arm movements is the highest treatment priority for people with paralysis, 6-fold higher than restoring walking ability. Nevertheless, current approaches to improve upper extremity function typically do not restore independence. Spinal cord stimulation is an emerging neuromodulation strategy to restore motor function. Recent studies using surgically implanted electrodes demonstrate impressive improvements in voluntary control of standing and stepping. Here we show that transcutaneous electrical stimulation of the spinal cord leads to rapid and sustained recovery of hand and arm function, even after complete paralysis. Notably, the magnitude of these improvements matched or exceeded previously reported results from surgically implanted stimulation. Additionally, muscle spasticity was reduced and autonomic functions including heart rate, thermoregulation, and bladder function improved. Perhaps most striking is that all six participants maintained their gains for at least three to six months beyond stimulation, indicating functional recovery mediated by long-term neuroplasticity. Several participants resumed their hobbies that require fine motor control, such as playing the guitar and oil painting, for the first time in up to 12 years since their injuries. Our findings demonstrate that non-invasive transcutaneous electrical stimulation of the spinal networks restores movement and function of the hands and arm for people with both complete paralysis and long-term spinal cord injury.

Brain-computer interfaces (BCIs) are an emerging strategy for spinal cord injury (SCI) intervention that may be used to reanimate paralyzed limbs. This approach requires decoding movement intention from the brain to control movement-evoking stimulation. Common decoding methods use spike-sorting and require frequent calibration and high computational complexity. Furthermore, most applications of closed-loop stimulation act on peripheral nerves or muscles, resulting in rapid muscle fatigue. Here we show that a local field potential-based BCI can control spinal stimulation and improve forelimb function in rats with cervical SCI. We decoded forelimb movement via multi-channel local field potentials in the sensorimotor cortex using a canonical correlation analysis algorithm. We then used this decoded signal to trigger epidural spinal stimulation and restore forelimb movement. Finally, we implemented this closed-loop algorithm in a miniaturized onboard computing platform. This Brain-Computer-Spinal Interface (BCSI) utilized recording and stimulation approaches already used in separate human applications. Our goal was to demonstrate a potential neuroprosthetic intervention to improve function after upper extremity paralysis.

Designing brain-computer interfaces (BCIs) that can be used in conjunction with ongoing motor behavior requires an understanding of how neural activity co-opted for brain control interacts with existing neural circuits. For example, BCIs may be used to regain lost motor function after stroke. This requires that neural activity controlling unaffected limbs is dissociated from activity controlling the BCI. In this study we investigated how primary motor cortex accomplishes simultaneous BCI control and motor control in a task that explicitly required both activities to be driven from the same brain region (i.e. a dual-control task). Single-unit activity was recorded from intracortical, multi-electrode arrays while a non-human primate performed this dual-control task. Compared to activity observed during naturalistic motor control, we found that both units used to drive the BCI directly (control units) and units that did not directly control the BCI (non-control units) significantly changed their tuning to wrist torque. Using a measure of effective connectivity, we observed that control units decrease their connectivity. Through an analysis of variance we found that the intrinsic variability of the control units has a significant effect on task proficiency. When this variance is accounted for, motor cortical activity is flexible enough to perform novel BCI tasks that require active decoupling of natural associations to wrist motion. This study provides insight into the neural activity that enables a dual-control brain-computer interface.

Innovations for creating somatosensation via direct electrical stimulation of the brain will be required for the next generation of bi-directional cortical neuroprostheses. The current lack of tactile perception and proprioceptive input likely imposes a fundamental limit on speed and accuracy of brain-controlled prostheses or re-animated limbs. This study addresses the unique challenge of identifying a robust, high bandwidth sensory encoding scheme in a high-dimensional parameter space. Previous studies demonstrated single dimensional encoding schemes delivering low bandwidth sensory information, but no comparison has been performed across parameters, nor with update rates suitable for real-time operation of a neuroprosthesis. Here, we report the first comprehensive measurement of the resolution of key stimulation parameters such as pulse amplitude, pulse width, frequency, train interval and number of pulses. Surprisingly, modulation of stimulation frequency was largely undetectable. While we initially expected high frequency content to be an ideal candidate for passing high throughput sensory signals to the brain, we found only modulation of very low frequencies were detectable. Instead, the charge-per-phase of each pulse yields the highest resolution sensory signal, and is the key parameter modulating perceived intensity. The stimulation encoding patterns were designed for high-bandwidth information transfer that will be required for bi-directional brain interfaces. Our discovery of the stimulation features which best encode perceived intensity have significant implications for design of any neural interface seeking to convey information directly to the brain via electrical stimulation.

Electrical intraspinal microstimulation (ISMS) at various sites along the cervical spinal cord permits forelimb muscle activation, elicits complex limb movements and may enhance functional recovery after spinal cord injury. Here, we explore optogenetic spinal stimulation (OSS) as a less invasive and cell type-specific alternative to ISMS. To map forelimb muscle activation by OSS in rats, adeno-associated viruses (AAV) carrying the blue-light sensitive ion channels channelrhodopsin-2 (ChR2) and Chronos were injected into the cervical spinal cord at different depths and volumes. Following an AAV incubation period of several weeks, OSS-induced forelimb muscle activation and movements were assessed at 16 sites along the dorsal surface of the cervical spinal cord. Three distinct movement types were observed. We find that AAV injection volume and depth can be titrated to achieve OSS-based activation of several movements. Optical stimulation of the spinal cord is thus a promising method for dissecting the function of spinal circuitry and targeting therapies following injury. NEW & NOTEWORTHY Optogenetics in the spinal cord can be used both for therapeutic treatments and to uncover basic mechanisms of spinal cord physiology. For the first time, we describe the methodology and outcomes of optogenetic surface stimulation of the rat spinal cord. Specifically, we describe the evoked responses of forelimbs and address the effects of different adeno-associated virus injection paradigms. Additionally, we are the first to report on the limitations of light penetration through the rat spinal cord.

Recent advances in neuroscience and devices are ushering in a new generation of medical treatments. Engineered biodevices are demonstrating the potential to create long-term changes in neural circuits, termed neuroplasticity. Thus, the approach of engineering neuroplasticity is rapidly expanding, building on recent demonstrations of improved quality of life for people with movement disorders, epilepsy, and spinal cord injury. In addition, discovering the fundamental mechanisms of engineered neuroplasticity by leveraging anatomically well-documented systems like the spinal cord is likely to provide powerful insights into solutions for other neurotraumas, such as stroke and traumatic brain injury, as well as neurodegenerative disorders, such as Alzheimer's, Parkinson disease, and multiple sclerosis. Now is the time for advancing both the experimental neuroscience, device development, and pioneering human trials to reap the benefits of engineered neuroplasticity as a therapeutic approach for improving quality of life after spinal cord injury.

Upper extremity function is the highest priority of tetraplegics for improving quality of life. We aim to determine the therapeutic potential of transcutaneous electrical spinal cord stimulation for restoration of upper extremity function. We tested the hypothesis that cervical stimulation can facilitate neuroplasticity that results in long-lasting improvement in motor control. A 62-year-old male with C3, incomplete, chronic spinal cord injury (SCI) participated in the study. The intervention comprised three alternating periods: 1) transcutaneous spinal stimulation combined with physical therapy (PT); 2) identical PT only; and 3) a brief combination of stimulation and PT once again. Following four weeks of combined stimulation and physical therapy training, all of the following outcome measurements improved: the Graded Redefined Assessment of Strength, Sensation, and Prehension test score increased 52 points and upper extremity motor score improved 10 points. Pinch strength increased 2- to 7-fold in left and right hands, respectively. Sensation recovered on trunk dermatomes, and overall neurologic level of injury improved from C3 to C4. Most notably, functional gains persisted for over 3 month follow-up without further treatment. These data suggest that noninvasive electrical stimulation of spinal networks can promote neuroplasticity and long-term recovery following SCI.

Paralysis due to spinal cord injury can severely limit motor function and independence. This review summarizes different approaches to electrical stimulation of the spinal cord designed to restore motor function, with a brief discussion of their origins and the current understanding of their mechanisms of action. Spinal stimulation leads to impressive improvements in motor function along with some benefits to autonomic functions such as bladder control. Nonetheless, the precise mechanisms underlying these improvements and the optimal spinal stimulation approaches for restoration of motor function are largely unknown. Finally, spinal stimulation may augment other therapies that address the molecular and cellular environment of the injured spinal cord. The fact that several stimulation approaches are now leading to substantial and durable improvements in function following spinal cord injury provides a new perspectives on the previously "incurable" condition of paralysis., (Copyright © 2017 the American Physiological Society.)

The number of clinical trials in regenerative medicine is burgeoning, and stem cell/tissue engineering technologies hold the possibility of becoming the standard of care for a multitude of diseases and injuries. Advances in regenerative biology reveal novel molecular and cellular targets, with potential to optimize tissue healing and functional recovery, thereby refining rehabilitation clinical practice. The purpose of this review is to (1) highlight the potential for synergy between the fields of regenerative medicine and rehabilitation, a convergence of disciplines known as regenerative rehabilitation; (2) provide translational examples of regenerative rehabilitation within the context of neuromuscular injuries and diseases; and (3) offer recommendations for ways to leverage activity dependence via combined therapy and technology, with the goal of enhancing long-term recovery. The potential clinical benefits of regenerative rehabilitation will likely become a critical aspect in the standard of care for many neurological and musculoskeletal disorders.

For brain-computer interfaces (BCIs) which provide the user continuous position control, there is little standardization of performance metrics or evaluative tasks. One candidate metric is Fitts's law, which has been used to describe aimed movements across a range of computer interfaces, and has recently been applied to BCI tasks. Reviewing selected studies, we identify two basic problems with Fitts's law: its predictive performance is fragile, and the estimation of 'information transfer rate' from the model is unsupported. Our main contribution is the adaptation and validation of an alternative model to Fitts's law in the BCI context. We show that the Shannon-Welford model outperforms Fitts's law, showing robust predictive power when target distance and width have disproportionate effects on difficulty. Building on a prior study of the Shannon-Welford model, we show that identified model parameters offer a novel approach to quantitatively assess the role of control-display gain in speed/accuracy performance tradeoffs during brain control.

Goal: To identify and overcome barriers to creating new neurotechnologies capable of restoring both motor and sensory function in individuals with neurological conditions., Methods: This report builds upon the outcomes of a joint workshop between the US National Science Foundation and the German Research Foundation on New Perspectives in Neuroengineering and Neurotechnology convened in Arlington, VA, USA, November 13-14, 2014., Results: The participants identified key technological challenges for recording and manipulating neural activity, decoding, and interpreting brain data in the presence of plasticity, and early considerations of ethical and social issues pertinent to the adoption of neurotechnologies., Conclusions: The envisaged progress in neuroengineering requires tightly integrated hardware and signal processing efforts, advances in understanding of physiological adaptations to closed-loop interactions with neural devices, and an open dialog with stakeholders and potential end-users of neurotechnology., Significance: The development of new neurotechnologies (e.g., bidirectional brain-computer interfaces) could significantly improve the quality of life of people living with the effects of brain or spinal cord injury, or other neurodegenerative diseases. Focused efforts aimed at overcoming the remaining barriers at the electrode tissue interface, developing implantable hardware with on-board computation, and refining stimulation methods to precisely activate neural tissue will advance both our understanding of brain function and our ability to treat currently intractable disorders of the nervous system.

Cervical spinal cord contusion is the most common human spinal cord injury, yet few rodent models replicate the pathophysiological and functional sequela of this injury. Here, we modified an electromechanical injury device and characterized the behavioral and histological changes occurring in response to a lateralized C4 contusion injury in rats. A key feature of the model includes a non-injurious touch phase where the spinal cord surface is dimpled with a consistent starting force. Animals were either left intact as a control, received a non-injury-producing touch on the surface of the cord ("sham"), or received a 0.6 mm or a 0.8 mm displacement injury. Rats were then tested on the forelimb asymmetry use test, CatWalk, and the Irvine, Beatties, and Bresnahan (IBB) cereal manipulation task to assess proximal and distal upper limb function for 12 weeks. Injuries of moderate (0.6 mm) and large (0.8 mm) displacement showed consistent differences in forelimb asymmetry, metrics of the CatWalk, and sub-scores of the IBB. Overall findings indicated long lasting proximal and distal upper limb deficits following 0.8 mm injury but transient proximal with prolonged distal limb deficits following 0.6 mm injury. Significant differences in loss of ipsilateral unmyelinated and myelinated white matter was detected between injury severities. Demyelination was primarily localized to the dorsolateral region of the hemicord and extended further rostral following 0.8 mm injury. These findings establish the C4 hemi-contusion injury as a consistent, graded model for testing novel treatments targeting forelimb functional recovery.

Neuroprosthetic approaches have tremendous potential for the treatment of injuries to the brain and spinal cord by inducing appropriate neural activity in otherwise disordered circuits. Substantial work has demonstrated that stimulation applied to both the central and peripheral nervous system leads to immediate and in some cases sustained benefits after injury. Here we focus on cervical intraspinal microstimulation (ISMS) as a promising method of activating the spinal cord distal to an injury site, either to directly produce movements or more intriguingly to improve subsequent volitional control of the paretic extremities. Incomplete injuries to the spinal cord are the most commonly observed in human patients, and these injuries spare neural tissue bypassing the lesion that could be influenced by neural devices to promote recovery of function. In fact, recent results have demonstrated that therapeutic ISMS leads to modest but sustained improvements in forelimb function after an incomplete spinal cord injury (SCI). This therapeutic spinal stimulation may promote long-term recovery of function by providing the necessary electrical activity needed for neuron survival, axon growth, and synaptic stability.

Transcranial ultrasound can alter brain function transiently and nondestructively, offering a new tool to study brain function now and inform future therapies. Previous research on neuromodulation implemented pulsed low-frequency (250-700 kHz) ultrasound with spatial peak temporal average intensities (ISPTA) of 0.1-10 W/cm(2). That work used transducers that either insonified relatively large volumes of mouse brain (several mL) with relatively low-frequency ultrasound and produced bilateral motor responses, or relatively small volumes of brain (on the order of 0.06 mL) with relatively high-frequency ultrasound that produced unilateral motor responses. This study seeks to increase anatomical specificity to neuromodulation with modulated focused ultrasound (mFU). Here, 'modulated' means modifying a focused 2-MHz carrier signal dynamically with a 500-kHz signal as in vibro-acoustography, thereby creating a low-frequency but small volume (approximately 0.015 mL) source of neuromodulation. Application of transcranial mFU to lightly anesthetized mice produced various motor movements with high spatial selectivity (on the order of 1 mm) that scaled with the temporal average ultrasound intensity. Alone, mFU and focused ultrasound (FUS) each induced motor activity, including unilateral motions, though anatomical location and type of motion varied. Future work should include larger animal models to determine the relative efficacy of mFU versus FUS. Other studies should determine the biophysical processes through which they act. Also of interest is exploration of the potential research and clinical applications for targeted, transcranial neuromodulation created by modulated focused ultrasound, especially mFU's ability to produce compact sources of ultrasound at the very low frequencies (10-100s of Hertz) that are commensurate with the natural frequencies of the brain.

When human hoppers are surprised by a change in surface stiffness, they adapt almost instantly by changing leg stiffness, implying that neural feedback is not necessary. The goal of this simulation study was first to investigate whether leg stiffness can change without neural control adjustment when landing on an unexpected hard or unexpected compliant (soft) surface, and second to determine what underlying mechanisms are responsible for this change in leg stiffness. The muscle stimulation pattern of a forward dynamic musculoskeletal model was optimized to make the model match experimental hopping kinematics on hard and soft surfaces. Next, only surface stiffness was changed to determine how the mechanical interaction of the musculoskeletal model with the unexpected surface affected leg stiffness. It was found that leg stiffness adapted passively to both unexpected surfaces. On the unexpected hard surface, leg stiffness was lower than on the soft surface, resulting in close-to-normal center of mass displacement. This reduction in leg stiffness was a result of reduced joint stiffness caused by lower effective muscle stiffness. Faster flexion of the joints due to the interaction with the hard surface led to larger changes in muscle length, while the prescribed increase in active state and resulting muscle force remained nearly constant in time. Opposite effects were found on the unexpected soft surface, demonstrating the bidirectional stabilizing properties of passive dynamics. These passive adaptations to unexpected surfaces may be critical when negotiating disturbances during locomotion across variable terrain.

A potential treatment for paralysis resulting from spinal cord injury is to route control signals from the brain around the injury by artificial connections. Such signals could then control electrical stimulation of muscles, thereby restoring volitional movement to paralysed limbs. In previously separate experiments, activity of motor cortex neurons related to actual or imagined movements has been used to control computer cursors and robotic arms, and paralysed muscles have been activated by functional electrical stimulation. Here we show that Macaca nemestrina monkeys can directly control stimulation of muscles using the activity of neurons in the motor cortex, thereby restoring goal-directed movements to a transiently paralysed arm. Moreover, neurons could control functional stimulation equally well regardless of any previous association to movement, a finding that considerably expands the source of control signals for brain-machine interfaces. Monkeys learned to use these artificial connections from cortical cells to muscles to generate bidirectional wrist torques, and controlled multiple neuron-muscle pairs simultaneously. Such direct transforms from cortical activity to muscle stimulation could be implemented by autonomous electronic circuitry, creating a relatively natural neuroprosthesis. These results are the first demonstration that direct artificial connections between cortical cells and muscles can compensate for interrupted physiological pathways and restore volitional control of movement to paralysed limbs.

Documenting the forelimb responses evoked by stimulating sites in primate cervical spinal cord is significant for understanding spinal circuitry and for potential neuroprosthetic applications involving hand and arm. We examined the forelimb movements and electromyographic (EMG) muscle responses evoked by intraspinal microstimulation in three M. nemestrina monkeys sedated with ketamine. Trains of three stimulus pulses (10-80 muA) at 300 Hz were delivered at sites in regularly spaced tracks from C6 to T1. Hand and/or arm movements were evoked at 76% of the 745 sites stimulated. Specifically, movements were evoked in digits (76% of effective sites), wrist (15% of sites), elbow (26%), and shoulder (17%). To document the muscle activity evoked by a stimulus current just capable of eliciting consistent joint rotation, stimulus-triggered averages of rectified EMG were calculated at each site where a movement was observed. Typically, many muscles were coactivated at threshold currents needed to evoke movements. Out of the 13-15 muscles recorded per animal, only one muscle was active at 14% of the effective sites and two to six muscles were coactivated at 47% of sites. Thus intraspinal stimulation at threshold currents adequate for evoking movement typically coactivated multiple muscles, including antagonists. Histologic reconstruction of stimulation sites indicated that responses were elicited from the dorsal and ventral horn and from fiber tracts in the white matter, with little somatotopic organization for movement or muscle activation. The absence of a clear somatotopic map of output sites is probably a result of the stimulation of complex mixtures of fibers and cells.

The Neurochip BCI is an autonomously operating interface between an implanted computer chip and recording and stimulating electrodes in the nervous system. By converting neural activity recorded in one brain area into electrical stimuli delivered to another site, the Neurochip BCI could form the basis for a simple, direct neural prosthetic. In tests with normal, unrestrained monkeys, the Neurochip continuously recorded activity of single neurons in primary motor cortex for several weeks at a time. Cortical activity was correlated with simultaneously-recorded electromyogram (EMG) activity from arm muscles during free behavior. In separate experiments with anesthetized monkeys, we found that microstimulation of the cervical spinal cord evoked movements of the arm and hand, often involving multiple muscles synergies. These observations suggest that spinal microstimulation controlled by cortical neurons could help compensate for damaged corticospinal projections.

The purpose of this study was to compare the influence of prolonged vibration of a hand muscle on the amplitude of the stretch reflex, motor unit discharge rate, and force fluctuations during steady, submaximal contractions. Thirty-two young adults performed 10 isometric contractions at a constant force (5.0 +/- 2.3% of maximal force) with the first dorsal interosseus muscle. Each contraction was held steady for 10 s, and then stretch reflexes were evoked. Subsequently, 20 subjects had vibration applied to the relaxed muscle for 30 min, and 12 subjects received no vibration. The muscle vibration induced a tonic vibration reflex. The intervention (vibration or no vibration) was followed by 2 sets of 10 constant-force contractions with applied stretches (After and Recovery trials). The mean electromyogram amplitude of the short-latency component of the stretch reflex increased by 33% during the After trials (P < 0.01) and by 38% during the Recovery trials (P < 0.01). The standard deviation of force during the steady contractions increased by 21% during the After trials (P < 0.05) and by 28% during the Recovery trials (P < 0.01). The discharge rate of motor units increased from 10.3 +/- 2.7 pulses/s (pps) before vibration to 12.2 +/- 3.1 pps (P < 0.01) during the After trials and to 11.9 +/- 2.6 pps during the Recovery trials (P < 0.01). There was no change in force fluctuations or stretch reflex magnitude for the subjects in the Control group. The results indicate that prolonged vibration increased the short-latency component of the stretch reflex, the discharge rate of motor units, and the fluctuations in force during contractions by a hand muscle. These adjustments were necessary to achieve the target force due to the vibration-induced decrease in the force capacity of the muscle.

Time- and frequency-domain measures of discharge times for pairs of motor units are used to infer the proportion of common synaptic input received by motor neurons. The physiological mechanisms that can produce the experimentally observed peaks in the cross-correlation histogram and the coherence spectrum are uncertain. The present study used a computational model to impose synchronization on the discharge times of motor units. Randomly selected discharge times of a unit that was being synchronized to a reference unit were aligned with some of the discharge times of the reference unit, provided the original discharge time was within 30 ms of the discharge by the reference unit. All time-domain measures (indexes CIS, E, and k') were sensitive to changes in the level of imposed motor-unit synchronization (P < 0.01). In addition, synchronization caused a peak between 16 and 32 Hz in the coherence spectrum. The shape of the cross-correlogram determined the frequency at which the peak occurred in the coherence spectrum. Further, the magnitude of the coherence peak was highly correlated with the time-domain measures of motor-unit synchronization (r2 > 0.80), with the highest correlation occurring for index E (r2 = 0.98). Thus the peak in the 16- to 32-Hz band of the coherence spectrum can be caused by the time that individual discharges are advanced or delayed to produce synchrony. Although the in vivo processes that adjust the timing of motor-unit discharges are not fully understood, these results suggest that they may not depend entirely on an oscillatory drive by the CNS.

The goal of this study was to improve the ability of a motor unit model to predict experimentally measured force variability across a wide range of forces. Motor unit discharge characteristics were obtained from 38 motor units of the first dorsal interosseus muscle. Motor unit discharges were recorded in separate isometric contractions that ranged from 4 to 85% of the maximal voluntary contraction (MVC) force above recruitment threshold. High-threshold motor units exhibited both greater minimal and peak discharge rates compared with low-threshold units (P < 0.01). Minimal discharge rate increased from 7 to 23 pps, and peak discharge rate increased from 14 to 38 pps with an increase in recruitment threshold. Relative discharge rate variability (CV) decreased exponentially for each motor unit from an average of 30 to 13% as index finger force increased above recruitment threshold. In separate experiments, force variability was assessed at eight force levels from 2 to 95% MVC. The CV for force decreased from 4.9 to 1.4% as force increased from 2 to 15% MVC (P < 0.01) and remained constant at higher forces (1.2-1.9%; P = 0.14). When the motor unit model was revised using these experimental findings, discharge rate variability was the critical factor that resulted in no significant difference between simulated and experimental force variability (P = 0.22) at all force levels. These results support the hypothesis that discharge rate variability is a major determinant of the trends in isometric force variability across the working range of a muscle.

During hopping in place and running, humans maintain similar center of mass dynamics by precisely adjusting leg mechanics to compensate for moderate changes in surface stiffness. We investigated the limits of this precise control by asking humans to hop in place on extremely soft elastic surfaces. We found that hoppers drastically altered leg mechanics and maintained similar center of mass dynamics despite a sevenfold change in surface stiffness (11-81 kN m(-1)). On the stiffest surfaces, the legs compressed in early stance and then extended in late stance in the pattern that is typical for normal bouncing gaits. On the softest surfaces, however, subjects reversed this pattern so that the legs extended up to 8 cm in early stance and then compressed by a similar distance in late stance. Consequently, the center of mass moved downward during stance by 5-7 cm less than the surface compressed and by a similar distance as on the stiffest surfaces. This unique leg action probably reduced extensor muscle pre-stretch because the joints first extended and then flexed during stance. This interpretation is supported by the observation that hoppers increased muscle activation by 50% on the softest surface despite similar joint moments and mechanical leg work as on the stiffest surface. Thus, the extreme adjustment to leg mechanics for very soft surfaces helps maintain normal center of mass dynamics but requires high muscle activation levels due to the loss of the normal extensor muscle stretch-shorten cycle.

Humans running and hopping maintain similar center-of-mass motions, despite large changes in surface stiffness and damping. The goal of this study was to determine the contributions of anticipation and reaction when human hoppers encounter surprise, expected, and random changes from a soft elastic surface (27 kN/m) to a hard surface (411 kN/m). Subjects encountered the expected hard surface on every fourth hop and the random hard surface on an average of 25% of the hops in a trial. When hoppers on a soft surface were surprised by a hard surface, the ankle and knee joints were forced into greater flexion by passive interaction with the hard surface. Within 52 ms after subjects landed on the surprise hard surface, joint flexion increased, and the legs became less stiff than on the soft surface. These mechanical changes occurred before electromyography (EMG) first changed 68-188 ms after landing. Due to the fast mechanical reaction to the surprise hard surface, center-of-mass displacement and average leg stiffness were the same as on expected and random hard surfaces. This similarity is striking because subjects anticipated the expected and random hard surfaces by landing with their knees more flexed. Subjects also anticipated the expected hard surface by increasing the level of EMG by 24-76% during the 50 ms before landing. These results show that passive mechanisms alter leg stiffness for unexpected surface changes before muscle EMG changes and may be critical for adjustments to variable terrain encountered during locomotion in the natural world.

Humans hopping and running on elastic and damped surfaces maintain similar center-of-mass dynamics by adjusting stance leg mechanics. We tested the hypothesis that the leg transitions from acting like an energy-conserving spring on elastic surfaces to a power-producing actuator on damped surfaces during hopping due to changes in ankle mechanics. To test this hypothesis, we collected surface electromyography, video kinematics, and ground reaction force while eight male subjects (body mass: 76.2 +/- 1.7 kg) hopped in place on a range of damped surfaces. On the most damped surface, most of the mechanical work done by the leg appeared at the ankle (52%), whereas 23 and 25% appeared at the knee and hip, respectively. Hoppers extended all three joints during takeoff further than they flexed during landing and thereby did more net positive work on more heavily damped surfaces. Also, all three joints reached peak flexion sooner after touchdown on more heavily damped surfaces. Consequently, peak moment occurred during joint extension rather than at peak flexion as on elastic surfaces. These strategies caused the positive work during extension to exceed the negative work during flexion to a greater extent on more heavily damped surfaces. At the muscle level, surface EMG increased by 50-440% in ankle and knee extensors as surface damping increased to compensate for greater surface energy dissipation. Our findings, and those of previous studies of hopping on elastic surfaces, show that the ankle joint is the key determinant of both springlike and actuator-like leg mechanics during hopping in place.

Fast-moving legged animals bounce along the ground with spring-like legs and agilely traverse variable terrain. Previous research has shown that hopping and running humans maintain the same bouncing movement of the body's centre of mass on a range of elastic surfaces by adjusting their spring-like legs to exactly offset changes in surface stiffness. This study investigated human hopping on damped surfaces that dissipated up to 72% of the hopper's mechanical energy. On these surfaces, the legs did not act like pure springs. Leg muscles performed up to 24-fold more net work to replace the energy lost by the damped surface. However, considering the leg and surface together, the combination appeared to behave like a constant stiffness spring on all damped surfaces. By conserving the mechanics of the leg-surface combination regardless of surface damping, hoppers also conserved centre-of-mass motions. Thus, the normal bouncing movements of the centre of mass in hopping are not always a direct result of spring-like leg behaviour. Conserving the trajectory of the centre of mass by maintaining spring-like mechanics of the leg-surface combination may be an important control strategy for fast-legged locomotion on variable terrain.