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.

After stroke bidirectional modulation of soleus stretch reflex amplitude emerges during rhythmic arm cycling.

OBJECTIVES: after stroke a typical presentation is exaggerated stretch reflexes (SRs) on the more affected (MA) side. The present study evaluated the contribution of presynaptic inhibition (PSI) induced by arm cycling and homosynaptic depression (HD) to the modulation of hyperreflexia at the ankle after stroke. Possible asymmetry of these effects between the MA and less affected (LA) legs was also assessed. METHODS: soleus SR was conditioned by: arm cycling at 1 Hz (to increase Ia PSI); or, a preceding conditioning tendon tap applied 1 s before the test stimulus (to induce HD). The extent of conditioning effects was compared between the MA and the LA legs. RESULTS: for both MA and LA legs, rhythmic arm movement induced a bidirectional effect in different participants, either increasing or decreasing SR amplitude (p < 0.05). HD had a significant effect in both legs (p < 0.05), however, the effect of both a previous muscle stretch and arm cycling was not different between the MA and the LA legs. CONCLUSION: our data reveal a bidirectional reflex modulation induced by arm cycling that produced facilitation in some and suppression in other participants after stroke. Relative SR amplitude modulation did not differ between the LA and MA legs. We speculate that alterations in SR amplitude modulation after stroke may reflect specific changes in both presynaptic afferent transmission mechanisms and fusimotor control. SIGNIFICANCE: the present findings open new perspectives on the characterization of pathophysiology of stroke during the performance of functionally relevant motor tasks.

Neural control of rhythmic, cyclical human arm movement: task dependency, nerve specificity and phase modulation of cutaneous reflexes.

1. The organization and pattern of cutaneous reflex modulation during rhythmic cyclical movements of the human upper limbs has received much less attention than that afforded the lower limb. Our working hypothesis is that control mechanisms underlying the modulation of cutaneous reflex amplitude during rhythmic arm movement are similar to those that control reflex modulation in the leg. Thus, we hypothesized that cutaneous reflexes would show task dependency and nerve specificity in the upper limb during rhythmic cyclical arm movement as has been demonstrated in the human lower limb. 2. EMG was recorded from 10 muscles crossing the human shoulder, elbow and wrist joints while bilateral whole arm rhythmic cyclical movements were performed on a custom-made, hydraulic apparatus. 3. Cutaneous reflexes were evoked with trains (5 x 1.0 ms pulses at 300 Hz) of electrical stimulation delivered at non-noxious intensities (approximately 2 x threshold for radiating parasthesia) to the superficial radial, median and ulnar nerves innervating the hand. 4. Cutaneous reflexes were typically modulated with the movement cycle (i.e. phase dependency was observed). There was evidence for nerve specificity of cutaneous reflexes during rhythmic movement of the upper limbs. Task-dependent modulation was also seen as cutaneous reflexes were of larger amplitude or inhibitory (reflex reversal) during arm cycling as compared to static contraction. 5. While there are some differences in the patterns of cutaneous reflex modulation seen between the arms and legs, it is concluded that cutaneous reflexes are modulated similarly in the upper and lower limbs implicating similar motor control mechanisms.

Human interlimb reflexes evoked by electrical stimulation of cutaneous nerves innervating the hand and foot.

There is some discrepancy over the extent to which reflex pathways from different cutaneous nerves in the hand and foot link the cervical and lumbar spinal cord in neurologically intact humans. The present experiments were designed to determine whether stimulation of a cutaneous nerve in the foot or in the hand evoked reflexes in the non-stimulated limbs (interlimb reflexes). Reflexes were elicited by stimulating (5x1-ms pulses at 300 Hz) the superficial peroneal (SP; innervates the foot dorsum) or superficial radial (SR; innervates the dorsolateral portion of the hand) nerve while subjects (n=10) performed focused contractions of different upper and lower limb muscles. Reflex responses were divided into early (<75 ms), middle (75-120 ms), and late (>120 ms) epochs as determined from averages of 50 sweeps of stimulus-locked electromyographic activity. Significant interlimb reflexes were found at the early latency in 44/106 and 44/103 muscles sampled after SP and SR nerve stimulation, respectively. At the middle latency, significant interlimb reflexes were seen in 89/106 and 87/103 muscles sampled after SP and SR nerve stimulation, respectively. Interlimb reflexes were seen when stimulating at the wrist (i.e. SR nerve) and when stimulating at the ankle (i.e. SP nerve) with an equal probability. The results show that interlimb cutaneous reflexes are widely distributed in humans. The mean latency of the earliest response was quite short and may be mediated by a propriospinal pathway. Functionally, these pathways may provide a substrate for transferring information to coordinate movements between the limb segments.

Differential regulation of cutaneous and H-reflexes during leg cycling in humans.

Reflexes undergo modulation according to task and timing during standing, walking, running, and leg cycling in humans. Both cutaneous and Hoffman (H-) reflexes are modulated by movement and task. However, recent evidence suggests that the modulation pattern for cutaneous and H-reflexes may be different. We sought to clarify this issue by reducing the effect of movement phase and altering the level of background muscle activation (low and high) in static and dynamic (leg cycling) conditions. Electromyography was recorded from the ankle extensors soleus and medial gastrocnemius (MG) and the knee extensor vastus lateralis (VL). Reflexes were evoked during the downstroke of stationary leg cycling. Cutaneous reflexes were evoked with trains of 5 x 1.0 ms pulses at 300 Hz delivered to the distal tibial nerve, whereas H-reflexes were evoked in soleus by stimulation with single 1.0-ms pulses. There were two main observations in this study: 1) middle latency cutaneous reflexes were facilitatory during static contraction but were dramatically attenuated or reversed to suppressive responses during cycling (task-dependent modulation); 2) soleus H-reflexes were larger in the high muscle activation condition but were unaffected by task (no task-dependent modulation). Thus opposite results were obtained in the two reflex pathways. It is concluded that cutaneous and H-reflexes are modulated by different mechanisms during active locomotor-like movements.

Modulation of human cutaneous reflexes during rhythmic cyclical arm movement.

The organization and pattern of cutaneous reflex modulation is unknown during rhythmic cyclical movements of the human upper limbs. On the assumption that these cyclic arm movements are central pattern generator (CPG) driven as has been suggested for leg movements such as walking, we hypothesized that cutaneous reflex amplitude would be independent of electromyographic (EMG) muscle activation level during rhythmic arm movement (phase-dependent modulation, as is often the case in the lower limb during locomotion). EMG was recorded from eight muscles crossing the human shoulder, elbow, and wrist joints while whole arm rhythmic cyclical movements were performed. Cutaneous reflexes were evoked with trains of electrical stimulation delivered at non-noxious intensities (approximately 2 x threshold for radiating paresthesia) to the superficial radial nerve innervating the lateral portion of the back of the hand. Phasic bursts of rhythmic muscle activity occurred throughout the movement cycle. Rhythmic EMG and kinematic patterns were similar to what has been seen in the human lower limb during locomotor activities such as cycling or walking: there were extensive periods of reciprocal activation of antagonist muscles. For most muscles, cutaneous reflexes were modulated with the movement cycle and were strongly correlated with the movement-related background EMG amplitude. It is concluded that cutaneous reflexes are primarily modulated by the background muscle activity during rhythmic human upper limb movements, with only some muscles showing phase-dependent modulation.

Absence of nerve specificity in human cutaneous reflexes during standing.

Cutaneous reflexes in lower limb muscles were recorded from healthy human subjects after non-noxious electrical stimulation of superficial peroneal (SP), sural and distal tibial nerves while subjects: (1) made graded voluntary contractions of the ankle and knee extensor and flexor muscles while mimicking late stance or heel strike limb positions; and (2) walked on a treadmill at speeds of 2 and 4 km/h. During standing, net reflexes were predominantly suppressive and graded with background EMG. In contrast, during walking net reflexes were mostly facilitatory and uncorrelated with background EMG. Opposite signs (negative during standing, positive during walking) and significant differences of the reflex ratio (net reflex/background EMG) were seen in most leg muscles. The nerve stimulated did not determine the sign of the net reflex while standing: nerve specificity was absent. We suggest that during standing, where maintenance of posture is of primary importance, there is a reduction of effort that led to increased cutaneous input (i.e., a global suppressive response), while during walking there is a modulation of reflexes which is independent of muscle activation level but closely tied to events occurring in the step cycle.

What functions do reflexes serve during human locomotion?

Studies on the reflex modulation of vertebrate locomotion have been conducted in many different laboratories and with many different preparations: for example, lamprey swimming, bird flight, quadrupedal walking in cats and bipedal walking in humans. Emerging concepts are that reflexes are task-, phase- and context-dependent. To function usefully in a behaviour such as locomotion wherein initial conditions change from step to step, reflexes would have to show modulation. Papers are reviewed in which the study of different reflexes have been conducted during different behaviours, with an emphasis on experiments in humans. A framework is developed in which the modulation and flexibility of reflexes are demonstrated. Alterations in cutaneous, and muscle (stretch and load receptor) reflexes between sitting, standing and walking are discussed. Studies in which both electrical, mechanical and 'natural' receptor activation have been conducted during walking are reviewed. Reflexes are shown to have important regulatory functions during human locomotion. A framework for discussion of reflex function throughout the step cycle is developed. The function of a given reflex pathway changes dynamically throughout the locomotor cycle. While all reflexes act in concert to a certain extent, generally cutaneous reflexes act to alter swing limb trajectory to avoid stumbling and falling. Stretch reflexes act to stabilize limb trajectory and assist force production during stance. Load receptor reflexes are shown to have an effect on both stance phase body weight support and step cycle timing. After neurotrauma or in disease, reflexes no longer function as during normal locomotion, but still have the potential to be clinically exploited in gait modification regimens.

Interaction of the Jendrássik maneuver with segmental presynaptic inhibition.

Since its initial description in 1883, the Jendrássik maneuver (JM) has been used in clinical neurological practice as an effective means of potentiating the tendon tap in neurologically impaired patients. The JM also potentiates its electrical analogue, the Hoffman (H-) reflex, but the mechanism of the reflex modulation has not been clearly established. We studied soleus H-reflex modulation in neurologically intact subjects while at rest and during a mild plantarflexion contraction (EMG level equivalent to approximately 10% maximum voluntary contraction). The control H-reflex was elicited by stimulating the tibial nerve in the popliteal fossa with single pulses of 1 ms duration. Conditioning of the reflex was by: (1) increasing segmental presynaptic inhibition via common peroneal nerve (CP) stimulation; (2) pulling the arms and clenching the teeth (JM); or (3) applying both together (JM+CP). CP stimulation significantly (P<0.05) suppressed the H-reflex (50% Hmax), while JM significantly (P<0.05) facilitated it during contraction. From either an analysis of the grouped data or by a within-subject analysis, we found that the combined effect of stimulating JM+CP was significantly lower than JM alone, but did not differ from control values or from CP alone. The simplest mechanism would be that the effects of the two sum algebraically on the interneurones producing segmental presynaptic inhibition of the H-reflex.

Function of sural nerve reflexes during human walking.

1. The functions of ipsilateral cutaneous reflexes were studied with short trains of stimuli presented pseudorandomly to the sural nerve during human walking. Electromyograms (EMG) of lower (tibialis anterior (TA), soleus, lateral (LG) and medial (MG) gastrocnemius) and upper leg (vastus lateralis and biceps femoris) muscles were recorded, together with ankle, knee and hip joint angles. Net reflex EMG responses were quantified in each of the sixteen parts of the step cycle. The kinematic measurements included ankle eversion- inversion, and ankle, knee and hip flexion-extension. 2. The function of the sural reflexes depended upon the part of the step cycle in which the nerve was stimulated and the intensity of stimulation. During stance, reflexes in MG and TA muscles in response to a medium intensity of stimulation (1.9 x radiating threshold, x RT) were closely associated with ankle eversion and dorsiflexion responses, respectively. These responses could assist in accommodation to uneven terrain that applies pressure to the lateral side of the foot (sural innervation area). Non-noxious, high intensity (2.3 x RT) stimulation resulted in strong suppression of LG and MG during stance which was correlated to a small reduction in ankle plantarflexion. At this higher intensity the response would function to prevent the foot from moving more forcefully onto a potentially harmful obstacle. 3. During swing, ankle dorsiflexion increased and was significantly correlated to the net TA EMG response after both medium and high intensity stimulation. Knee flexion was increased throughout swing at both intensities of stimulation. These responses may serve in an avoidance response in which the swing limb is brought past an obstacle without destabilizing contact. 4. The net EMG and kinematic responses suggest that cutaneous reflexes stabilize human gait against external perturbations produced by an uneven surface in stance or obstacles encountered during swing.

Reflexes from the superficial peroneal nerve during walking in stroke subjects.

The function of ipsilateral cutaneous reflexes was studied with short trains of stimuli presented pseudorandomly to the superficial peroneal nerve (SP; innervates the top of the foot) during treadmill walking in neurologically intact (NI) subjects and subjects who had had a stroke. Ankle and knee joint angles together with electromyograms (EMG) of tibialis anterior (TA), soleus (SOL), medial gastrocnemius (MG), vastus lateralis (VL), and biceps femoris (BF) muscles were recorded. Net reflex EMG and kinematic responses to stimulation were quantified in each of the 16 parts of the step cycle and responses compared between the stroke and NI subjects. Stimulation strongly suppressed extensor muscles throughout stance in the stroke subjects. TA muscle showed a significant suppression during swing phase that was correlated with reduced ankle dorsiflexion in both stroke and NI subjects. BF reflexes were facilitatory during parts of swing and VL reflexes were suppressive throughout stance in the stroke subjects. There was a significant correlation between BF facilitation and knee flexion during swing, which was stronger in NI subjects. We conclude that only part of the stumble correction to foot dorsum electrical stimulation observed in NI subjects is maintained after stroke, and that new, suppressive responses are seen.

Ballistic movement performance in karate athletes.

Nine male karate athletes and 13 untrained men did maximal voluntary isometric (MVC) and ballistic elbow extension actions, the latter unloaded (L0) and against a load equal to 10% MVC (L10). The karate group achieved greater (P < 0.05) isometric (32%) and ballistic action peak torque with L0 (30%) and L10 (40%). With L10 the ratio of ballistic action to isometric action, peak torque was 13% greater in the karate group, indicating a load specific training adaptation. With L0 the corresponding ratio did not differ significantly between groups. Ballistic action peak rate of torque development (51%, 51%) and peak acceleration (15%, 9%) with L0 and L10, respectively, were greater in the karate group. In contrast, peak velocity and movement time did not differ significantly between groups. Electromyographic recordings of agonist triceps and antagonist biceps were made during the isometric and ballistic actions. Since ballistic actions (L10) were initiated from a preloaded condition, the occurrence and duration of premovement agonist depression were monitored. In ballistic actions there were no group differences in agonist activation, the ratio of ballistic to isometric action agonist activation, or antagonist coactivation. Premovement agonist depression occurred infrequently in both groups, with no group differences. It is concluded that karate athletes have enhanced elbow extension ballistic performance, but it could not be related to amplified agonist activation, altered antagonist activation, or more frequent occurrence of agonist premovement depression.

Reproducibility of ballistic movement.

The reproducibility of ballistic actions performed on a custom-made apparatus was assessed in six untrained men who reported to the laboratory two times over a span of 10 d, on each occasion performing three isometric maximal voluntary contractions (MVC, elbow extension) and 10 ballistic elbow extension movements in each of two conditions: unloaded (L0) and with a load equal to 10% MVC (L10). For both the average of the trials and the best trial, method errors and Pearson correlation coefficients (r) were calculated for isometric peak torque and 10 (5 at each of L0 and L10) selected ballistic movement parameters (peak torque, peak rate of torque development, movement time, peak velocity, and peak acceleration). Based on method errors obtained and given an alpha level of 0.05 and power of 0.9, needed sample sizes were calculated for treatment effects ranging from 5 to 20%. Method errors for isometric peak torque were 5.1 and 3.1% for best and average of trials, respectively. For the 10 ballistic parameters, the corresponding method errors averaged 7.1 +/- 5.4% (SD) and 6.8 +/- 3.6%. The largest method errors were found in peak torque and peak rate of torque development with L0. The expected high negative correlation between method errors and r values was not found. For 5, 10, and 20% treatment effects, 4, 6, and 9 of 10 best trial measures met the sample size criterion of N < or = 20. For the average of trials, 3, 8, and all 10 met the criterion. With the exception of rate of torque development, the reproducibility of the described ballistic measures is acceptable for longitudinal training studies and cross-sectional group comparisons.

Cutaneous reflexes during human gait: electromyographic and kinematic responses to electrical stimulation.

The functions of ipsilateral cutaneous reflexes were studied with short trains of stimuli presented pseudorandomly to the superficial peroneal (SP) and tibial nerves during human gait. Electromyograms (EMGs) of tibialis anterior (TA), soleus, lateral and medial gastrocnemius, vastus lateralis (VL), and biceps femoris (BF) muscle were recorded, together with ankle and knee joint angles. Net reflex EMG responses were quantified in each of the 16 parts of the step cycle according to a recently developed technique. After SP nerve stimulation, TA muscle showed a significant suppression during swing phase that was highly correlated to ankle plantarflexion. BF and VL muscles were both excited throughout swing and significantly correlated to knee flexion during early swing. Tibial nerve stimulation caused dorsiflexion during late stance, but plantarflexion during late swing. We argue that SP nerve reflexes are indicative of a stumbling corrective response to nonnoxious electrical stimulation in humans. The correlated kinematic responses after tibial nerve stimulation may allow smooth movement of the swing leg so as to prevent tripping during swing and to assist placing and weight acceptance at the beginning of stance.

Estimating mechanical parameters of leg segments in individuals with and without physical disabilities.

Methods are described for estimating the inertia, viscosity, and stiffness of the lower leg around the knee and of the whole leg around the hip that are applicable even to persons with considerable spasticity. These involve: 1) a "pull" test in which the limb is slowly moved throughout its range of motion while measuring angles (with an electrogoniometer) and torques (with a hand-held dynamometer) to determine passive stiffness and 2) a "pendulum" test in which the limb is moved against gravity and then dropped, while again measuring angles and torques. By limiting the extent of the movement and choosing a direction (flexion or extension) that minimizes reflex responses, the mechanical parameters can be determined accurately and efficiently using computer programs. In the sample of subjects studied (nine with disability related to spinal cord injury, head injury, or stroke, and nine with no neurological disability), the inertia of the lower leg was significantly reduced in the subjects with disability (p < 0.05) as a result of atrophy, but the stiffness and viscosity were within normal limits. The values of inertia were also compared with anthropometric data in the literature. The identification of these passive parameters is particularly important in designing systems for functional electrical stimulation of paralyzed muscles, but the methods may be widely applicable in rehabilitation medicine.

Ballistic movement: muscle activation and neuromuscular adaptation.

Movements that are performed with maximal velocity and acceleration can be considered ballistic actions. Ballistic actions are characterized by high firing rates, brief contraction times, and high rates of force development. A characteristic triphasic agonist/antagonist/agonist electromyographic (EMG) burst pattern occurs during ballistic movement, wherein the amount and intensity of antagonist coactivation is variable. In conditions of low-grade tonic muscular activity, a premovement EMG depression (PMD; or silent period, PMS) can occur in agonist muscles prior to ballistic contraction. The agonist PMD period may serve to potentiate the force and velocity of the following contraction. A selective activation of fast twitch motor units may occur in ballistic contractions under certain movement conditions. Finally, high-velocity ballistic training induces specific neuromuscular adaptations that occur as a function of the underlying neurophysiological mechanisms that subserve ballistic movement.

Oxygen uptake, heartrate and blood lactate responses to the Chito-Ryu Seisan kata in skilled karate practitioners.

To evaluate the efficacy of Seisan kata as an aerobic power training mode, four male (28.5 +/- 4.2 y) Chito-Ryu karate black belt practitioners did kata continuously for 10 min. In separate sessions the kata (formal, organized movement sequences) were done at rates of 1 (PACE) and 2 (FAST) kata "cycles" per minute. Heartrate (HR) and VO2 were monitored continuously during the sessions. VO2 during the PACE and FAST sessions averaged 73 +/- 3 and 94 +/- 2% of leg cycling VO2peak, respectively. The corresponding HRs were 93 +/- 6 and 101 +/- 3% of HRmax (leg cycle test). PACE and FAST post-exercise blood lactates were 12 +/- 4 and 22 +/- 6%, respectively, of the maximal leg cycle test values. These data indicate that karate kata can be used as an effective and specific means for training aerobic power in karate practitioners.