Pedaling improves gait ability of hemiparetic patients with stiff-knee gait: fall prevention during gait

Background and PurposeStiff-knee gait, which is a gait abnormality observed after stroke, is characterized by decreased knee flexion angles during the swing phase, and it contributes to a decline in gait ability. This study aimed to identify the immediate effects of pedaling exercises on stiff-knee gait from a kinesiophysiological perspective.MethodsTwenty-one patients with chronic post-stroke hemiparesis and stiff-knee gait were randomly assigned to a pedaling group and a walking group. An ergometer was set at a load of 5 Nm and rotation speed of 40 rpm, and gait was performed at a comfortable speed; both the groups performed the intervention for 10 min. Kinematic and electromyographical data while walking on flat surfaces were immediately measured before and after the intervention.ResultsIn the pedaling group, activity of the rectus femoris significantly decreased from the pre-swing phase to the early swing phase during gait after the intervention. Flexion angles and flexion angular velocities of the knee and hip joints significantly increased during the same period. The pedaling group showed increased step length on the paralyzed side and gait velocity.ConclusionsPedaling increases knee flexion during the swing phase in hemiparetic patients with stiff-knee gait and improves gait ability.     

Hip-phase-dependent flexion reflex modulation and expression of spasms in patients with spinal cord injury

The flexion reflex in human spinal cord injury (SCI) is believed to incorporate interneuronal circuits that consist elements of the stepping generator while ample evidence suggest that hip proprioceptive input is a controlling signal of locomotor output. In this study, we examined the expression of the non-nociceptive flexion reflex in response to imposed sinusoidal passive movements of the ipsilateral hip in human SCI. The flexion reflex was elicited by low-intensity stimulation (300 Hz, 30 ms pulse train) of the right sural nerve at the lateral malleolus, and recorded from the tibialis anterior (TA) muscle. Sinusoidal hip movements were imposed to the right hip joint at 0.2 Hz by a Biodex system while subjects were supine. The effects of leg movement on five leg muscles along with hip, knee, and ankle joint torques were established simultaneously with the modulation pattern of the flexion reflex during hip oscillations. Phase-dependent modulation of the flexion reflex was present during hip movement, with the reflex to be significantly facilitated during hip extension and suppressed during hip flexion. The phase-dependent flexion reflex modulation coincided with no changes in TA pre- and post-stimulus background ongoing activity during hip extension and flexion. Reflexive muscle and joint torque responses, induced by the hip movement and substantiated by excitation of flexion reflex afferents, were entrained to specific phases of hip movement. Joint torque responses were consistent with multi-joint spasmodic muscle activity, which was present mostly during the transition phase of the hip from flexion to extension and from mid- to peak extension. Our findings provide further evidence on the interaction of hip proprioceptors with spinal interneuronal circuits engaged in locomotor pathways, and such interaction should be considered in rehabilitation protocols employed to restore sensorimotor function in people with SCI.     

Electromyographic evaluation of the sound and involved side during gait of spastic hemiplegic children with cerebral palsy

The purpose of this study was to investigate the surface electromyogram (EMG) of the lower limbs of hemiplegic children with spastic cerebral palsy during gait. The EMG of seven muscles was analyzed for 17 children (5-12 years old). The EMG of the involved side was decreased for the examined shank muscles and increased for the hamstrings, during certain phases of the gait cycle, compared with the sound side. The rectus femoris of the involved side showed prolonged activation during the swing phase. The enhanced activation of the hamstrings may be beneficial/compensatory, preventing knee hyperextension. The presence of equinus foot obstructs the foot clearance and hence the prolonged rectus femoris EMG activity during the swing phase may contribute to shorten the lower limb by flexing the hip. Possible compensatory mechanisms of the proximal muscles of the involved lower limb that can be measured with instrumented gait analysis should be taken into account before the decision for a specific treatment.     

Parallel facilitatory reflex pathways from the foot and hip to flexors and extensors in the injured human spinal cord

Spinal integration of sensory signals associated with hip position, muscle loading, and cutaneous sensation of the foot contributes to movement regulation. The exact interactive effects of these sensory signals under controlled dynamic conditions are unknown. The purpose of the present study was to establish the effects of combined plantar cutaneous afferent excitation and hip movement on the Hoffmann (H) and flexion reflexes in people with a spinal cord injury (SCI). The flexion and H-reflexes were elicited through stimulation of the right sural (at non-nociceptive levels) and posterior tibial nerves respectively. Reflex responses were recorded from the ipsilateral tibialis anterior (TA) (flexion reflex) and soleus (H-reflex) muscles. The plantar cutaneous afferents were stimulated at three times the perceptual threshold (200 Hz, 24-ms pulse train) at conditioning-test intervals that ranged from 3 to 90 ms. Sinusoidal movements were imposed to the right hip joint at 0.2 Hz with subjects supine. Control and conditioned reflexes were recorded as the hip moved in flexion and extension. Leg muscle activity and sagittal-plane joint torques were recorded. We found that excitation of plantar cutaneous afferents facilitated the soleus H-reflex and the long latency flexion reflex during hip extension. In contrast, the short latency flexion reflex was depressed by plantar cutaneous stimulation during hip flexion. Oscillatory joint forces were present during the transition phase of the hip movement from flexion to extension when stimuli were delivered during hip flexion. Hip-mediated input interacts with feedback from the foot sole to facilitate extensor and flexor reflex activity during the extension phase of movement. The interactive effects of these sensory signals may be a feature of impaired gait, but when they are appropriately excited, they may contribute to locomotion recovery in these patients.     

RECTUS FEMORIS TRANSFER TO IMPROVE KNEE FUNCTION OF CHILDREN WITH CEREBRAL PALSY

Stance phase stability and swing phase clearance, prerequisites for normal ambulation, often are lost in the gait of children with cerebral palsy. Lengthening of the hamstrings usually will improve stance-phase knee extension but will not greatly alter swing-phase knee flexion. This paper presents the outcome of transfer of the distal end of the rectus femoris in conjunction with hamstrings lengthening in 37 knees, and compares it with a control group of 24 knees in which only hamstrings lengthening was done. In the first group swing-phase knee flexion was improved by 16.0 +/- 14.4 degrees, compared to 9.5 +/- 7.5 degrees in the control group, and residual knee flexion in stance was reduced to 8.9 +/- 8.1 degrees, compared to 15.1 +/- 13.8 degrees in the controls. Poor outcome in the transfer-plus-lengthening group was associated mainly with foot rotation in excess of 8 degrees internally or externally, or postoperative knee flexion in stance. Criteria for selection of cases and methods of improving surgical outcome are discussed.     

Clinical relevance of gait research applied to clinical trials in spinal cord injury

The restoration of walking function following SCI is extremely important to consumers and has stimulated a response of new treatments by scientists, the pharmaceutical industry and clinical entrepreneurs. Several of the proposed interventions: (1) the use of functional electrical stimulation (FES) and (2) locomotor training have been examined in clinical trials and recent reviews of the scientific literature. Each of these interventions is based on research of human locomotion. Therefore, the systematic study of walking function and gait in normal individuals and those with injury to the spinal cord has contributed to the identification of the impairments of walking, the development of new treatments and how they will be measured to determine effectiveness. In this context gait research applied to interventions to improve walking function is of high clinical relevance. This research helps identify walking impairments to be corrected and measures of walking function to be utilized as endpoints for clinical trials. The most common impairments following SCI diagnosed by observational gait analysis include inadequate hip extension during stance, persistent plantar flexion and hip/knee flexion during swing and foot placement at heel strike. FES has been employed as one strategy for correcting these impairments based on analysis that range from simple measures of speed, cadence and stride length to more sophisticated systems of three- dimensional video motion analysis and multichannel EMG tracings of integrated walking. A recent review of the entire FES literature identified 36 studies that merit comment and the full range of outcome measures for walking function were used from simple velocity to the video analysis of motion. In addition to measures of walking function developed for FES interventions, the first randomized multicenter clinical trial on locomotor training in subacute SCI was recently published with an extensive review of these measures. In this study outcome measures of motor strength (impairment), balance, Walking Index for SCI (WISCI), speed, 5min walk (walking capacities) and locomotor functional independence measure (L-FIM), a disability measure all showed improvement in walking function based on the strategy of the response of activity based plasticity to step training. Although the scientific basis for this intervention will be covered in other articles in this series, the evolution of clinical outcome measures of walking function continues to be important for the determination of effectiveness in clinical trials.     

Hip angle induced modulation of H reflex amplitude, latency and duration in spinal cord injured humans.

OBJECTIVES: To investigate the modulation of the soleus H reflex in spinal cord injured (SCI) subjects resulting from imposed changes in hip angle and to establish whether changes in H reflex amplitude co-vary with changes in reflex latency and duration. METHODS: H reflexes were recorded using conventional methods in 7 SCI subjects in the supine position. The right leg was secured by a leg brace and positioned at various angles of hip flexion (30 degrees, 40 degrees ) and at 10 degrees of hip extension. RESULTS: We found that imposing 10 degrees of hip extension resulted in a significant facilitation in the size of the soleus H reflex in all of the SCI subjects tested (200% of control reflex; recorded at 10 degrees of hip flexion). In contrast, positioning the hip at 30 degrees and at 40 degrees of flexion resulted in a significant reduction of the H reflex in 6 of 7 SCI subjects tested. In the remaining subject, an increase in the H reflex amplitude was observed. Modulation of H reflex amplitude coincided with shifts in both H reflex latency and duration. The reflex latency was prolonged when the reflex amplitude was reduced following hip flexion, while hip extension shortened the reflex latency. In contrast, the H reflex duration was prolonged with hip extended and shortened with hip flexed. CONCLUSIONS: When changes in static hip joint position are imposed in SCI subjects, changes in afferent feedback from hip proprioceptors are capable of promoting a switch between excitatory and inhibitory pathways. Associated changes in H reflex latency and duration are consistent with the hypothesis that oligosynaptic inputs contribute to the hip angle-induced H reflex modulation. Possible mechanisms for these effects are discussed.     

Gait patterns of a patient with myoclonus of a lower limb,when OFF and ON treatment with antiepileptic drugs

Abstract We describe kinematics, kinetics and electromyographic patterns of a patient with spinal myoclonus of the left lower limb, during walking. Gait analysis was performed when the patient was OFF and ON his treatment with antiepileptic drugs. When OFF, we mainly observed clonic bursts and out-of-phase activations of m. tibialis anterior and m. rectus femoris, with increased hip flexion, reduction of knee flexion during swing and excessive ankle dorsal flexion. Furthermore, large oscillations of knee moment of force and power during stance phase were also observed. These abnormal patterns markedly recovered when ON drugs.     

Expansion of nociceptive withdrawal reflex receptive fields in spinal cord injured humans

OBJECTIVE: In spinal cord injured (SCI) subjects, exaggerated withdrawal reflexes associated with a dominant flexor pattern irrespective of stimulation site have been reported. In the present study, withdrawal reflex receptive field (RRF) was determined in complete SCI subjects (N=9). METHODS: Distributed electrical stimulation was applied to the sole of the foot, and reflexes in tibialis anterior, soleus, biceps femoris, and vastus lateralis muscles were recorded together with knee and ankle movement trajectories. A group of spinally intact subjects (N=10) were included as controls. With the subjects in supine position, stimulation was applied to 10 different sites on the foot sole. Based on the tibialis anterior reflex threshold for stimulation on the mid foot sole, two stimulus intensities (1.1 times the reflex threshold and 1.4 times the reflex threshold) were used for all 10 sites. RESULTS: In SCI subjects, dorsi-flexion dominated independent of stimulus site and the tibialis anterior RRF covered the entire foot sole in contrast to a well-defined tibialis anterior receptive field at the medial, distal foot sole in the spinally intact subjects. Further, the soleus RRF also covered the entire sole in the SCI subjects. The reflexes in biceps femoris and vastus lateralis muscles were small and associated with weak knee flexion at all 10 sites in the SCI subjects and in the controls. CONCLUSIONS: The RRF of the ankle flexor and the ankle extensor muscles both covered the entire sole of the foot indicating an expansion of the RRFs following spinal cord injury. The expansion is most likely due to lack of descending inhibitory control and/or increased sensitivity of the spinal reflex loop in the SCI subjects. SIGNIFICANCE: The study improves the understanding of spinal reflex control in spinal intact and spinal cord injured subjects.     

Is the modified Tardieu scale in semi‐standing position better associated with knee extension and hamstring activity in terminal swing than the supine Tardieu?

The aim of this study was to investigate whether the modified Tardieu scale (MTS) in a semi-standing position, used for the assessment of hamstrings spasticity, was better associated with knee extension and hamstrings activity in terminal swing than the MTS in a supine position in children with cerebral palsy (CP). Seven children diagnosed with spastic CP (Gross Motor Function Classification System Levels I-II) and seven healthy comparison children participated in the study. An instrumented MTS in supine and semi-standing position and an instrumented gait assessment were conducted. Results showed that spasticity-related outcomes of the semi-standing MTS do not show better associations with terminal swing characteristics of gait than the same outcomes of the supine MTS in children with spastic CP. Only the passive restricted knee angle from the supine MTS was strongly associated with the maximum knee extension during gait (r(s)=0.99; p <0.001), suggesting that hamstrings length is more important for terminal swing behaviour than hamstrings spasticity.     

Reflex effects of induced muscle contraction in normal and spinal cord injured subjects

The modulation of the soleus H reflex in response to functional electrical stimulation (FES) of the rectus femoris (RF) muscle and its overlying skin was examined in 11 normal adults and 6 patients with a clinically defined complete spinal cord injury (SCI). Stimulation of RF at twice motor threshold (MT) resulted in a long-lasting (>1,000 ms) and significant reduction (50-70% of control) in the size of the soleus H reflex in all normal subjects tested. For five of the SCI subjects, 2MT stimulation of RF induced a 55-60% reduction in the soleus H reflex that was also long-lasting (>160 ms). In the remaining SCI subject, 2MT stimulation resulted in an initial period of significant H-reflex facilitation (0-14 ms) that was followed by a longer-lasting inhibition commencing 60 ms after the cessation of the conditioning stimulation. Decreasing the strength of stimulation to below that required to generate a clear contraction in RF resulted in mixed facilitatory and inhibitory actions that were subject dependent. The changes in H-reflex excitability resulting from FES highlight the potential use of FES in the management of hypertonicity in SCI but also suggest that the central actions of FES need to be considered when FES gait restoration programs are designed.     

Reflex responses of human thigh muscles to non-noxious sural stimulation during stepping

An investigation of reflex responses of leg muscles to sural stimulation during stepping was performed on human subjects. Non-noxious electrical stimulation applied during the swing phase or the latter half of the stance phase produced a mixed increase and decrease of EMG activity in the hamstring muscles. No response or very weak response was observed when the same stimulus was applied during either quiet standing or various levels of constant voluntary effort at varying hip and knee joint angles.     

Reflex component of the swing phase: a comparative analysis of locomotion in intact and deafferentated rats

Comparative analysis of hindlimb biomechanics and EMG activity with different kinds of locomotion before and after bilateral LI-S2 spinal cord deafferentation were performed in rats. A delay of the onset and increase of duration of knee and ankle joint flexion, but not hip joint flexion were revealed after deafferentation. It was accompanied by reinforcing of the F-period of the swing phase which was more prominent during walking than swimming. The amplitude and duration of the muscle activity decreased, in particular, during the F-period of the swing phase. The role of afferent inflow in the formation of the F-phase of the locomotor cycle is discussed.     

Cognitive tuning of corticospinal excitability during human gait: adaptation to the phase

The aim of this study was to investigate how the cognitive tuning of corticospinal (CS) excitability adapts to the type of evoked-movement (Flexion vs. Extension) during human gait. Transcranial magnetic stimulation (TMS) was used both as a central perturbation evoking a movement and as a tool for quantifying the CS excitability of the muscles under study (RF/BF). In the first condition (Dst), the TMS occurred at mid-stance, inducing hip extension, whereas in the second condition (Dsw), the TMS occurred at the beginning of the swing phase, inducing hip flexion. In both conditions, the subjects were asked to cognitively prepare to either not intervene (NINT) or to compensate (COMP) for the evoked-movements. The results showed that, regardless of the type of evoked-movement, preparing to compensate resulted in a selective increase in the CS excitability to those muscles that would be involved in counteracting the possible central perturbation, i.e. the hip extensor muscle (BF) to compensate for an evoked flexion during the swing phase or the hip flexor muscle (RF) to compensate for an evoked extension during the stance phase. This latter result offers the first evidence of a modulation in CS excitability to the proximal muscles during the stance phase. In conclusion, the cognitive tuning of CS excitability was found to adapt to the gait phases. Moreover, the same selective preparation strategy was observed whether the central perturbation occurred during the stance or the swing phase of the step cycle.     

Quantitative assessment of knee extensor thrust,flexed-knee gait,insufficient knee flexion during the swing phase,and medial whip in hemiplegia using three-dimensional treadmill gait analysis

Background: Most people with hemiplegia experience gait changes after a stroke. Abnormal gait patterns in stroke patients vary across subjects and this make it difficult to assess the cause of gait abnormalities. Therefore, it is necessary to quantitatively evaluate abnormal gait patterns through gait analysis for stroke patients.

Objective: To develop and evaluate the validity of quantitative assessments of the degree of knee extensor thrust, flexed-knee gait, insufficient knee flexion during the swing phase, and medial whip.

Methods: Forty-six healthy control subjects and 112 people with hemiplegia participated. From the 112 patients, 50 patients were selected into each abnormal gait pattern (knee extensor thrust, flexed-knee gait, insufficient knee flexion during the swing phase, and medial whip) with some overlap. Participants were instructed to walk on a treadmill and were recorded using a three-dimensional motion analysis system. An index to quantify each of the four abnormal gait patterns exhibited by the patients was calculated from the three-dimensional coordinate data. The indices were developed based on the definition of the abnormal gait patterns. The index values for the patients were compared with those of healthy subjects as well as with the results of observational gait assessment by three physical therapists with expertise in gait analysis.

Results: Strong correlation was observed between the index value and the median observational rating for all four abnormal gait patterns (?0.64 to ?0.86). Most of the patients with an abnormal gait pattern had a higher index value than the healthy subjects.

Conclusions: The use of these indices in gait analysis of people with hemiplegia can help to diagnose severity of gait disorder, determine the appropriate treatment, and evaluate the effectiveness of the treatment.     

Reduction of seating pressure using FES in patients with spinal cord injury. A preliminary report.

The aim of this study was to investigate the use of functional electrical stimulation (FES) as a means of pressure sore prevention in seated spinal cord injured (SCI) subjects. Nine SCI subjects took part in tests in which electrical stimulation was applied to the quadriceps with the lower legs restrained. Ischial pressures were measured during periods of quiet sitting and FES application. A strain gauged lever arm was used to measure the knee moment during quadriceps stimulation. The average pressure drop at the right and left buttocks was 44 mmHg and 27 mmHg respectively. In general the greatest reductions occurred in subjects with larger knee moments; however, there was no direct relationship between the pressure reduction obtained and the quadriceps strength. This form of FES may be useful as a prophylactic aid in the management of pressure sores in SCI subjects.     

On-line flexibility of the cognitive tuning of corticospinal excitability: a TMS study in human gait

Human subjects have been found to be able to cognitively prepare themselves to resist to a TMS-induced central perturbation by selectively modulating the corticospinal excitability (CS). The aim of this study was to investigate the on-line adaptability of this cognitive tuning of CS excitability during human gait. Transcranial magnetic stimulation (TMS) was used both as a central perturbation evoking a movement and as a tool for quantifying the CS excitability before the movement was evoked. TMS was applied at mid-stance (evoking additional hip extension) or at the beginning of the swing (evoking hip flexion) with a random phase, thus evoking unpredictable flexion or extension movement. This was compared to a condition of fixed phase, in which the subjects knew in advance the direction of the evoked movement. In both conditions, we compared the amplitude of the TMS-evoked movement and the motor-evoked potentials (MEPs) of the muscles acting at the hip joint (RF/BF) according to two opposite instructions, either to cognitively prepare to "let go", or to cognitively prepare to "compensate" for the evoked movements. The results showed that the subjects were able to compensate for random TMS-evoked movements, but with a lower performance level in comparison to the fixed TMS-evoked movements. When they succeeded in the random-phase condition, the subjects used the same preparation strategy as in the fixed-phase condition; preparing to compensate resulted in a selective increase in the CS excitability to those muscles which would be involved in counteracting the possible central perturbation. This requires continuous change in the tuning of CS excitability within the stride and thus reveals the high flexibility of the cognitive tuning of CS excitability during gait.     

Pre- and post-alpha motoneuronal control of the soleus H-reflex during sinusoidal hip movements in human spinal cord injury

The aim of this study was to establish the contribution of hip-mediated sensory feedback to spinal interneuronal circuits during dynamic conditions in people with incomplete spinal cord injury (SCI). Specifically, we investigated the effects of synergistic and antagonistic group I afferents on the soleus H-reflex during imposed sinusoidal hip movements. The soleus H-reflex was conditioned by stimulating the common peroneal nerve (CPN) at short (2, 3, and 4 ms) and long (80, 100, and 120 ms) conditioning test (C-T) intervals to assess the reciprocal and pre-synaptic inhibition of the soleus H-reflex, respectively. The soleus H-reflex was also conditioned by medial gastrocnemius (MG) nerve stimulation at C-T intervals ranging from 4 to 7 ms to assess changes in autogenic Ib inhibition during hip movement. Sinusoidal hip movements were imposed to the right hip joint at 0.2 Hz by the Biodex system while subjects were supine. The effects of sinusoidal hip movement on five leg muscles along with hip, knee, and ankle joint torques were also established during sensorimotor conditioning of the reflex. Phase-dependent modulation of antagonistic and synergistic muscle afferents was present during hip movement, with the reciprocal, pre-synaptic, and Ib inhibition to be significantly reduced during hip extension and reinforced during hip flexion. Reflexive muscle and joint torque responses--induced by the hip movement--were entrained to specific phases of hip movement. This study provides evidence that hip-mediated input acts as a controlling signal of pre- and post-alpha motoneuronal control of the soleus H-reflex. The expression of these spinal interneuronal circuits during imposed sinusoidal hip movements is discussed with respect to motor recovery in humans after SCI.     

Effect of multilevel botulinum toxin a and comprehensive rehabilitation on gait in cerebral palsy

To evaluate the effect of multilevel botulinum toxin A and comprehensive rehabilitation on gait pattern, muscle length, and spasticity, a multicenter randomized trial was performed in 46 children with spastic cerebral palsy who walk with flexed knees. Their mean age was 8.0 years (range 4 to 11 years). They were randomly allocated to the intervention group (multilevel botulinum toxin A and comprehensive rehabilitation) or the control group (usual care). After 6 weeks, a significant treatment effect in the intervention group was observed on: improved knee extension during midstance and terminal swing (7 degrees and 5 degrees , P < 0.01, respectively); hip rotation during terminal swing (4 degrees , P = 0.02); gait score (1.7, P < 0.01); decreased spasticity in hamstrings (11 degrees , P < 0.01), gastrocnemius (6 degrees , P = 0.01), and soleus (5 degrees , P = 0.02); and increased muscle length in hamstrings (9 degrees , P < 0.01) and gastrocnemius (5 degrees , P < 0.01). The improved muscle length was maintained up to 24 weeks. This study demonstrated that multilevel botulinum toxin A and comprehensive rehabilitation improves knee extension during gait, increases muscle length, and decreases spasticity in injected muscles after 6 weeks in children who walk with flexed knees. Although the effect on muscle length was maintained after 24 weeks, the effect on gait and spasticity had disappeared.     

Single joint perturbation during gait: preserved compensatory response pattern in spinal cord injured subjects.

OBJECTIVE: Responses to afferent input during locomotion are organized at the spinal level but modulated by supraspinal centers. The study aim was to examine whether supraspinal influences affect the behavior of complex electromyographic (EMG) responses to single limb perturbations during walking. METHODS: Subjects with motor-complete (MCSCI), motor-incomplete spinal cord injury (MISCI), and non-disabled (ND) subjects participated. Hip or knee joint trajectory was briefly arrested by a robotic device at early or late swing phase. EMG responses from muscles of both legs were analyzed. RESULTS: Perturbation-induced EMG responses of spinal cord injured and ND individuals were similar in basic structure, with the exception that tibialis anterior onset times were delayed for SCI subjects. Across all groups, perturbations in late swing (i.e., near the swing-to-stance transition) were associated with shorter muscle onset times and higher EMG amplitudes. Knee perturbations were associated with shorter muscle response onset times, while hip perturbations elicited higher response amplitudes. EMG responses were also evoked in muscles contralateral to the perturbation. CONCLUSIONS: These data indicate that neuronal circuits within the spinal cord deprived of normal supraspinal input respond to swing phase perturbations in a manner that is similar to that of the intact spinal cord. SIGNIFICANCE: The adult human spinal cord is capable of generating complex, phase-appropriate responses much as has been observed in studies of human infants and in spinal animals.