Neuromechanical interactions between the limbs during human locomotion: an evolutionary perspective with translation to rehabilitation.

During bipedal locomotor activities, humans use elements of quadrupedal neuronal limb control. Evolutionary constraints can help inform the historical ancestry for preservation of these core control elements support transfer of the huge body of quadrupedal non-human animal literature to human rehabilitation. In particular, this has translational applications for neurological rehabilitation after neurotrauma where interlimb coordination is lost or compromised. The present state of the field supports including arm activity in addition to leg activity as a component of gait retraining after neurotrauma.

Adaptation of cutaneous stumble correction when tripping is part of the locomotor environment.

We recently showed that cutaneous reflexes evoked by stimulating the superficial peroneal (SP; innervates foot dorsum) nerve are modulated according to the level of postural threat. Context-related modulation was observed mainly in contralateral (c) responses but not in the ipsilateral responses. This lack of effect on ipsilateral (i) cutaneous reflexes might have been caused by the general nature of the whole body perturbation. We therefore hypothesized that context-relevant mechanical perturbations applied to the dorsum of the foot by an instrumented rod at early swing during walking would produce differences in ipsilateral cutaneous reflex amplitudes, consistent with the functional relevance of the SP nerve in stumble correction responses. Subjects walked on a motorized treadmill under four conditions: 1) normal, 2) normal with mechanical perturbations at the foot dorsum, 3) arms crossed, and 4) arms crossed with mechanical perturbations at the foot dorsum. Electrical stimulation of the SP nerve was delivered at five phases of the step cycle, and cutaneous reflexes were compared between all conditions for each phase of the step cycle. Reflex responses were generally found to be modulated in amplitude during walking conditions in which mechanical perturbations were delivered, particularly in ipsilateral tibialis anterior (iTA), which showed a marked reduction in inhibition. The results indicated cutaneous reflexes in iTA and contralateral medial gastrocnemius (cMG) were influenced by the threat of a trip, induced by applying mechanical perturbations to the foot dorsum during walking. This task-related gating of cutaneous reflexes was not generalized to all muscles, thus suggesting a functional role in the maintenance of stability during locomotion.

Context-dependent modulation of interlimb cutaneous reflexes in arm muscles as a function of stability threat during walking.

Cutaneous reflexes evoked in the muscles of the arms with electrical stimulation of nerves of the foot ("interlimb reflexes") are observed during walking. These reflexes have been suggested to coordinate the actions of the legs and arms when walking is disturbed. Recently, we showed that cutaneous reflexes evoked in the leg muscles after stimulation at the foot are modulated according to the level of postural threat during walking. We hypothesized that the amplitude of interlimb cutaneous reflexes would similarly be modulated when subjects walk in unstable environments. Subjects walked on a treadmill under four walking conditions: 1) normal; 2) normal with unpredictable anterior-posterior (AP) perturbations; 3) arms crossed; and 4) arms crossed with unpredictable AP perturbations. Interlimb reflexes evoked from electrical stimulation of the right superficial peroneal or sural nerves were recorded bilaterally, at four points of the step cycle. These reflexes were compared between conditions in which the arms were moving in a similar manner: 1) normal versus AP walking and 2) arms crossed versus arms crossed with AP perturbations. Differences in reflex amplitudes between arms-crossed conditions were observed in most upper limb muscles when subjects were perturbed while walking compared with undisturbed walking. This effect was less apparent when the arms were swinging freely. The results indicate that the strength of interlimb connections is influenced by the level of postural threat (i.e., the context of the behavior), thereby suggesting that these reflexes serve a functional link between the legs and arms during locomotion.

Postural uncertainty leads to dynamic control of cutaneous reflexes from the foot during human walking.

Cutaneous reflexes evoked by stimulation of nerves innervating the foot are modulated in a phase-dependent manner during locomotion. The pattern of modulation of these reflexes has been suggested to indicate a functional role of cutaneous reflexes in assisting to maintain stability during walking. We hypothesized that if cutaneous reflexes assist in maintaining stability during gait, then these reflexes should be modulated in a context-dependent manner when subjects are asked to walk in an environment in which stability is challenged. To do this, we asked subjects to walk on a treadmill under five conditions: (1) normally, (2) with the arms crossed, (3) while receiving unpredictable anterior-posterior (AP) perturbations, (4) with the arms crossed while receiving unpredictable AP perturbations, and (5) with the hands holding onto fixed handles. Cutaneous reflexes arising from electrical stimulation of the superficial peroneal (SP; relevant to stumbling) or distal tibial (TIB; relevant to ground contact sensation) nerves were recorded bilaterally, at four points in the step cycle. Reflexes evoked with SP nerve stimulation showed marked facilitation during the most unstable walking condition in 4 of the 7 muscles tested. SP nerve-evoked reflexes in the muscles of the contralateral leg also showed suppression during the most stable walking condition. Reflexes evoked with TIB nerve stimulation were less affected by changes in the walking task. We argue that the specific adaptation of cutaneous reflexes observed with SP nerve stimulation supports the hypothesis that cutaneous reflexes from the foot contribute to the maintenance of stability during walking.

Possible contributions of CPG activity to the control of rhythmic human arm movement.

There is extensive modulation of cutaneous and H-reflexes during rhythmic leg movement in humans. Mechanisms controlling reflex modulation (e.g., phase- and task-dependent modulation, and reflex reversal) during leg movements have been ascribed to the activity of spinal central pattern generating (CPG) networks and peripheral feedback. Our working hypothesis has been that neural mechanisms (i.e., CPGs) controlling rhythmic movement are conserved between the human lumbar and cervical spinal cord. Thus reflex modulation during rhythmic arm movement should be similar to that for rhythmic leg movement. This hypothesis has been tested by studying the regulation of reflexes in arm muscles during rhythmic arm cycling and treadmill walking. This paper reviews recent studies that have revealed that reflexes in arm muscles show modulation within the movement cycle (e.g., phase-dependency and reflex reversal) and between static and rhythmic motor tasks (e.g., task-dependency). It is concluded that reflexes are modulated similarly during rhythmic movement of the upper and lower limbs, suggesting similar motor control mechanisms. One notable exception to this pattern is a failure of contralateral arm movement to modulate reflex amplitude, which contrasts directly with observations from the leg. Overall, the data support the hypothesis that CPG activity contributes to the neural control of rhythmic arm movement.

Coordinated interlimb compensatory responses to electrical stimulation of cutaneous nerves in the hand and foot during walking.

It has been shown that stimulation of cutaneous nerves innervating the hand (superficial radial, SR) and foot (superficial peroneal, SP) elicit widespread reflex responses in many muscles across the body. These interlimb reflex responses were suggested to be functionally relevant to assist in motor coordination between the arms and legs during motor tasks such as walking. The experiments described in this paper were conducted to test the hypothesis that interlimb reflexes were phase-dependently modulated and produced functional kinematic changes during locomotion. Subjects walked on a treadmill while electromyographic (EMG) activity was collected continuously from all four limbs, and kinematic recordings were made of angular changes across the ankle, knee, elbow, and shoulder joints. Cutaneous reflexes were evoked by delivering trains of electrical stimulation pseudorandomly to the SP nerve or SR nerves in separate trials. Reflexes were phase-averaged according to the time of occurrence in the step cycle, and phasic amplitudes and latencies were calculated. For both nerves, significant phase-dependent modulation (including reflex reversals) of interlimb cutaneous reflex responses was seen in most muscles studied. Both SR and SP nerve stimulation resulted in significant alteration in ankle joint kinematics. The results suggest coordinated and functionally relevant reflex pathways from the SP and SR nerves onto motoneurons innervating muscles in nonstimulated limbs during walking, thus extending observations from the cat to that of the bipedal human.

Modulation of cutaneous reflexes in arm muscles during walking: further evidence of similar control mechanisms for rhythmic human arm and leg movements.

Stimulation of cutaneous nerves innervating the hand evokes prominent reflexes in many arm muscles during arm cycling. We hypothesized that the mechanisms controlling reflex modulation during the rhythmic arm swing of walking would be similar to that documented during arm cycling. Thus, we expected cutaneous reflexes to be modulated by position in the walking cycle (phase dependence) and be different when walking compared to contraction while standing (task dependence). Subjects performed static postures similar to those occurring during walking and also walked on a treadmill while the superficial radial nerve was electrically stimulated pseudorandomly throughout the step cycle. EMG was recorded bilaterally from upper limb muscles and kinematic recordings were obtained from the elbow and shoulder joints. Step cycle information was obtained from force-sensing insoles. Analysis was conducted after averaging contingent upon the occurrence of stimulation in the step cycle. Phase-dependent modulation of cutaneous reflexes at early (approximately 50-80 ms) and middle (approximately 80-120 ms) latencies was observed. Coordinated bilateral reflexes were seen in posterior deltoid and triceps brachii muscles. Task dependency was seen in that reflex amplitude was only correlated with background EMG during static contraction (75% of comparisons for both early and middle latency reflexes). During walking, no significant relationship between reflex amplitude and background EMG level was found. The results show that cutaneous reflex modulation during rhythmic upper limb movement is similar to that seen during arm cycling and to that observed in leg muscles during locomotion. These results add to the evidence that, during cyclical movements of the arms and legs, similar neural mechanisms observed only during movement (e.g. central pattern generators) control reflex output.