Sensori-sensory afferent conditioning with leg movement: gain control in spinal reflex and ascending paths.

Studies are reviewed, predominantly involving healthy humans, on gain changes in spinal reflexes and supraspinal ascending paths during passive and active leg movement. The passive movement research shows that the pathways of H reflexes of the leg and foot are down-regulated as a consequence of movement-elicited discharge from somatosensory receptors, likely muscle spindle primary endings, both ipsi- and contralaterally. Discharge from the conditioning receptors in extensor muscles of the knee and hip appears to lead to presynaptic inhibition evoked over a spinal path, and to long-lasting attenuation when movement stops. The ipsilateral modulation is similar in phase to that seen with active movement. The contralateral conditioning does not phase modulate with passive movement and modulates to the phase of active ipsilateral movement. There are also centrifugal effects onto these pathways during movement. The pathways of the cutaneous reflexes of the human leg also are gain-modulated during active movement. The review summarizes the effects across muscles, across nociceptive and non-nociceptive stimuli and over time elapsed after the stimulus. Some of the gain changes in such reflexes have been associated with central pattern generators. However, the centripetal effect of movement-induced proprioceptive drive awaits exploration in these pathways. Scalp-recorded evoked potentials from rapidly conducting pathways that ascend to the human somatosensory cortex from stimulation sites in the leg also are gain-attenuated in relation to passive movement-elicited discharge of the extensor muscle spindle primary endings. Centrifugal influences due to a requirement for accurate active movement can partially lift the attenuation on the ascending path, both during and before movement. We suggest that a significant role for muscle spindle discharge is to control the gain in Ia pathways from the legs, consequent or prior to their movement. This control can reduce the strength of synaptic input onto target neurons from these kinesthetic receptors, which are powerfully activated by the movement, perhaps to retain the opportunity for target neuron modulation from other control sources.

Aging of human segmental oligosynaptic reflexes for control of leg movement.

A heteronymous group I oligosynaptic reflex from the common peroneal nerve to vastus medialis muscle was compared with a group I homonymous monosynaptic reflex to soleus, using electrical stimulation of peripheral nerve trunks in two groups of healthy men, mean ages 22 and 65 years. The oligosynaptic reflex was still elicitable with age, its magnitude decreasing similarly to the monosynaptic reflex. A further group of older subjects, mean age 75 years, showed similar results. Clearly, the oligosynaptic reflex is not lost with healthy aging. The motor interneuronal pool may at least partially avoid the age-related cell loss of motoneuronal pools, with consequent maintenance of segmental participation for movements such as gait. The slowing of conduction velocities, for these proprioceptive reflex arcs, may reduce the effectiveness of autoregulation of the gait.

Task-relevant selective modulation of somatosensory afferent paths from the lower limb.

Leg movement attenuates initial somatosensory evoked potentials (SEPS) from both cutaneous and muscle afferent origin. To date, as different sensory inputs become relevant for task performance, selective facilitation from such movement-related gating influences has not been shown. We hypothesized that initial SEP amplitudes from cutaneous (sural nerve, SN) and muscle afferent (tibial nerve, TN) sources are dependent on the relevance of the specific afferent information to task performance. SEPs were obtained at rest and during three movement conditions. In each movement condition, the left foot was passively moved episodically and additional cutaneous 'codes' of sensory information were applied to the dorsum of the left foot. Subjects were instructed to: simply relax (passive), or to make a response following the cessation of movement, dependent either on the cutaneous code (cutaneous task), or the passive movement trajectory of the left foot (position task). Passive movement, with no required subsequent response, attenuated initial TN and SN SEPs to approximately 40% of that at rest (p < 0.05). Versus passive movement, when cutaneous inputs provided the relevant cue for the task, mean SN SEPs significantly increased (p < 0.05), and when the proprioceptive inputs provided the relevant cue for the task, mean TN SEPs significantly increased (p < 0.05). We conclude that specific relevancy of sensory information selectively facilitates somatosensory paths from movement-related attenuation.

Phasic modulation of somatosensory potentials during passive movement.

Tibial nerve somatosensory evoked potential (SEP) amplitude modulates to passive stretch of leg extensors with movement, paralleling spinal reflex modulation. We therefore hypothesized that SEP amplitude is phasically attenuated during flexion in passive pedalling. SEPs and soleus H reflexes were evoked at four phase positions when the leg was static and passively moved. Initial SEPs were attenuated at full flexion compared with extension for both conditions (p < 0.05). SEPs during movement were significantly lower than those in the static condition (p < 0.05). There were no significant movement or phase effects on subsequent SEP components. H reflex modulation resembled that for initial SEPs. We conclude that movement-induced amplitude modulation of initial SEPs arises, partly, from phasic discharge of extensor muscle spindles.

Temporal properties of attention sharing consequent to disturbed balance.

The time course and extent of attentional shifts associated with compensatory balancing reactions were explored using a novel dual-task paradigm. Seated subjects performed a continuous visuomotor tracking task with the hand while the feet simultaneously balanced an inverted pendulum. The pendulum was randomly perturbed, evoking compensatory balance reactions. Changes in tracking performance were held to reflect attentional shifts. Discrete deviation in visuomotor tracking, typically a pause in tracking, began on average 235 ms after the onset of the balance reaction (TA EMG; average latency 90 ms). Such pauses lasted on average 600 ms, although additional errors in tracking lasted up to 9 s following the perturbation. The findings reveal evidence of dynamic shifts in attention associated with distinct phases of compensatory balance control. The initial phase appears to be triggered automatically, whereas later phases involve varying degrees of attentional resources.

A technique for electrically induced perturbation of rhythmic leg movement.

The paper describes electrical circuitry which replaces a mechanical brake, for perturbation of the contractile load of the legs during pedalling. The turning flywheel of an ergometer is connected to an alternator, with the electrical load provided by a power resistor connected across the output terminals. A 12-V battery provides the field current. Through variable resistors the field current is altered under microprocessor control, providing different steady-state loads when pedalling and also sudden transient changes of load. The point of change in load in the movement cycle can be accurately selected. The ergometer is instrumented for accurate measurement of pedal crank position, crank angular velocity and reaction force at the foot, to provide a physical description of the evoked steady states and transients, using microprocessor controlled sampling. The results show that the technique has application to the study of the range of reflex responses within a movement cycle and also to the more complex restoration of a movement pattern over a number of cycles. It is applicable to investigation of normal and diseased states.

Response synergies over a single leg when it is perturbed during the complex rhythmic movement of pedalling.

Previous studies report that perturbing the posture of humans evokes specific patterns of muscular synergies in the legs. This study investigated the pattern of muscular responses of a whole limb when it was rapidly perturbed in the phase of extending during stationary pedalling. Subjects were instructed to resist. Accordingly, we anticipated increased extensor activity at knee and ankle to overcome the perturbation. This did not occur in the initial responses, appearing at latencies of 85-132 ms (mean = 104 ms). In contrast, there was facilitation in tibialis anterior, and the knee extensors vastus medialis and rectus femoris, together with profound inhibition of the ankle extensors soleus and lateral gastrocnemius. The anticipated extensor response across the limb appeared in the subsequent pattern of electromyogram (EMG) activity, with latencies ranging from 121 to 195 ms (mean = 168 ms), together with a large increase in propulsive force on the pedal. The difference in EMG patterns and latencies between initial and subsequent synergies was used to separate the responses into an earlier 'prevolitional' and a later 'volitional' component.

Movement-induced depression of soleus H reflexes is consistent in humans over the range of excitatory afferents involved.

The presumption that the H reflex arises exclusively from Ia afferent discharge has been challenged. If the reflex is comprised of many afferent responses, then movement-induced H reflex inhibition witnessed at one point in the recruitment curve may be quite different from the inhibition at another point in the curve. H reflex recruitment curves were constructed for three subjects during passive pedalling, isolated knee rotation and isolated hip rotation. Compared to control recruitment curves, these curves were reduced across the full spectrum of stimulus intensities. This suggests one of two possibilities: (1) all afferents contributing to the H reflex are subject to the same source and modality of inhibition; or (2) there is only one afferent type contributing to the reflex.

Movement features and H-reflex modulation. I. Pedalling versus matched controls.

Modulation of soleus H-reflex magnitude over a cycle of leg movement and the adjustment of controls to account for it were explored. During pedalling, H-reflex magnitudes in all nine subjects were highest in the power producing phase and lowest in recovery. Stimulation intensity was standardized. Compared to sitting, these reflexes were significantly depressed (P less than 0.05). The sitting condition was modified in one experiment, so that the angles of the limb joints and the contraction level of soleus were matched to their values, measured at 13 equi-spaced points, around the pedal cycle. This matching resulted in some modulation of the H-reflex around the pedal cycle, when sitting. When the contraction of tibialis anterior was added to these changes to the seated control, this modulation came closer to that seen during movement. Movement-specific modulation of the reflex was now harder to identify. These data raise the question of whether the three features presently used for matching are causative in the movement modulation of the soleus H-reflex and whether they represent effects arising from centrally descending or peripheral sources.

Movement features and H-reflex modulation. II. Passive rotation, movement velocity and single leg movement.

Modulation of soleus H-reflex magnitudes during pedalling, and their approximation when seated with appropriate joint positions and contractile activity was demonstrated in the previous paper. The present study investigated the modulation of H-reflexes during (A) pedalling movement in the absence of contractile activity, (B) different movement velocities and (C) movement of a single limb. Using a customized tandem cycle ergometer, seated subjects with trunk supported relaxed their leg muscles and allowed their legs to be rotated. Their feet were supported on the pedals with the ankle braced. Reflexes were collected at four phases in the movement cycle (with some at 13 phases) and with speeds of 5-60 revolutions per min (cycle times from 12 to 1 s). The results showed that (i) reflex magnitude substantially decreased with limb rotation (P less than 0.05). The degree of inhibition was dependent on the phase position. (ii) Increasing speed of passive rotation increased the inhibition at all positions, but was most pronounced near the fullest flexion of hip and knee. When subjects actively pedalled, the relationship between speed and inhibition remained. (iii) When the contralateral leg was moved and the target leg was stationary, crossed projection of reflex inhibition was clear. (iv) The reflex gain measured during active pedalling of one leg was similar to that observed during two legged pedalling. Again, a crossed effect from the contralateral leg could be observed. We conclude that the net influence of discharge from movement-elicited afference is inhibitory on this reflex path and that the reflex modulation during pedalling arises from overlaid sources.(ABSTRACT TRUNCATED AT 250 WORDS)

The relationship between the kinematics of passive movement, the stretch of extensor muscles of the leg and the change induced in the gain of the soleus H reflex in humans.

The gain of the H reflex attenuates during passive stepping and pedalling movements of the leg. We hypothesized that the kinematics of the movement indirectly reflect the receptor origin of this attenuation. In the first experiment, H reflexes were evoked in soleus at 26 points in the cycle of slow, passive pedalling movement of the leg and at 13 points with the leg static (the ankle was always immobilized). Maximum inhibition occurred as the leg moved through its most flexed position (P < 0.05). Inhibition observed in the static leg was also strongest at this position (P < 0.05). The increase in inhibition was gradual during flexion movement, with rapid reversal of this increase during extension. In the second experiment, the length of stretch of the vasti muscles was modelled. Variable pedal crank lengths and revolutions per minute (rpm) altered leg joint displacements and angular velocities. Equivalent rates of stretch of the vasti, achieved through different combinations of joint displacements and velocities, elicited equivalent attenuations of mean reflex magnitudes in the flexed leg. Reflex gain exponentially related to rate of stretch (R2 = 0.98 P < 0.01). The results imply that gain attenuation of this spinal sensorimotor path arises from spindle discharge in heteronymous extensor muscles of knee and/or hip, concomitant with movement.

Movement-induced modulation of soleus H reflexes with altered length of biarticular muscles.

Passive pedaling movements of the leg results in the phasic modulation of the soleus H reflex of that leg. In contrast, the H reflex of the contralateral leg is attenuated tonically. The phasic modulation of the reflex ipsilaterally can be attributed to the afferent discharge associated with the cyclic lengthening of the extensor muscles. We hypothesized that the tonic attenuation of the contralateral reflex could be explained if the afferent feedback arising from the lengthening of the biarticular muscles had an increased importance in regulating the amplitude of the contralateral reflex. To test this, the passive pedaling movements were reduced to those about either the knee or hip alone. Despite the alteration in the pattern of stretching of the biarticular muscles, the contralateral soleus H reflex was tonically attenuated during both forms of single joint movements. We suggest that the same phasic afferent discharge responsible for the modulation of the ipsilateral soleus H reflex initiates the tonic attenuation contralaterally, but that the signal undergoes a complex transformation in crossing the cord. These results do not rule out the possibility that the stretching of the biarticular muscles contributes to the attenuation of the ipsilateral soleus H reflex, which is subsequently masked by a powerful influence from the stretching of the uniarticular extensor muscles. To test this possibility, a second experiment manipulated the lengths of the muscles of the leg by altering the positions of the static joints during isolated rotation of either the knee or hip and measuring the amplitude of the ipsilateral soleus H reflex. From the results, it was clear that stretching the uniarticular extensor muscles produced the most dramatic effects. However, the stretch of the biarticular muscles yielded mild inhibitory influences if these muscles were near their maximal lengths.

Modulation of human short latency reflexes between standing and walking.

Inhibition of the magnitude of soleus muscle homonymous (H) reflexes occurs in humans when walking, compared to standing. The current study asked, (1) was the task modulation of Ia reflexes limited to soleus muscle, (2) was there support for attributing a presynaptic source to the inhibition in humans and (3) did an oligosynaptic short latency reflex show similar task modulation? In 3 subjects, H reflexes were evoked in vastus medialis and soleus, at 4 levels of contraction in the target muscle, with constant stimulus intensity when walking and standing. The reflex magnitudes in both muscles were significantly inhibited during the contractions for walking, compared to standing. Such inhibition also occurred in H reflexes of tibialis anterior muscle. An excitatory oligosynaptic reflex was then evoked in vastus medialis, through low intensity stimulation of the common peroneal nerve during walking and standing. The mean amplitudes of this reflex were not significantly different (P less than 0.05) between the two conditions, at any contraction level. The depression of quadriceps H reflexes, compared to the oligosynaptic reflexes through the same quadriceps motoneuronal pool in the same task, strongly suggested that the inhibition of H reflexes arose at other sites besides the motoneuronal cell body and proximal dendrites. We conclude that Ia H reflexes of various leg muscles of humans are inhibited when walking but that this does not generalize to the oligosynaptic short latency reflex between the anterior shank and thigh.

Contralateral inhibition of soleus H reflexes with different velocities of passive movement of the opposite leg.

The research question was, do events arising from rhythmic passive movement of the human leg lead to inhibition of the H reflex pathway in the stationary leg contralateral to that movement? Further, as the angular velocity of the passive movement increases, does the contralateral reflex inhibition also increase? Stable stimulation of the tibial nerve elicited H reflexes in the EMG of soleus. Trials involved the stimulated or the contralateral leg being rotated passively in a pedalling motion, at various velocities. The controls were made with the subjects seated and relaxed. The results showed that reflex magnitudes were significantly depressed when the test limb was passively rotated at 60 rpm. in comparison to the seated control trials. Rotation of the opposite limb depressed reflex magnitudes in the test limb, which was stationary. This contralateral inhibition increased, (mean reflex magnitudes of 62.68%, 41.04%, 16.65% and 9.58% of peak-to-peak Mmax), as the velocity of rotation of the opposite limb increased (10, 30, 60, 90 rpm, respectively) (P < 0.01). The effect of movement velocity was interpreted as the result of altered sensory receptor discharge arising from the passive movement. It is concluded that contralateral sensory activity contributes to the movement-elicited afferent discharge which tunes the spinal somatosensory-motor mechanisms for human locomotion.

Crossed inhibition of the soleus H reflex during passive pedalling movement.

We hypothesized that sensory input from the moving leg induces presynaptic inhibition of the soleus H reflex pathway in the contralateral stationary leg. The results showed a crossed inhibition during passive pedalling movement of the leg, which was not removed by low levels of tonic contraction of soleus in the stationary leg. The inhibition was correlated exponentially to the rate of the movement (R2 = 0.934, P < 0.05) and was not dependent on the quadrants through which the moving leg was passing. Static flexion of the stationary leg caused ipsilateral inhibition of the reflexes (t = 5.590, P < 0.05), independent of the orientations of the other leg. We concluded that sensory inflow from the moving leg induces presynaptic inhibition in the stationary leg, that a complex transformation of the sensory input in the spinal cord or brain underlies the tonic crossed inhibition and phasic ipsilateral inhibition, and that descending motor commands exert a powerful control over these sensorimotor modulatory mechanisms.

The afferent origin of the secondary somatosensory evoked potential from the lower limb in humans.

The afferent origin of the secondary somatosensory evoked potential elicited from stimulation of the sural and tibial nerves was investigated as the limb was cooled. It was hypothesized that the peak of this potential is initiated from primary afferents in the A alpha group. We conclude that the peak of the secondary SEP arises from an afferent source whose diameter is of similar size to that of large diameter A alpha afferents.

Mechanisms within the human spinal cord suppress fast reflexes to control the movement of the legs.

Passive locomotor-like movement induces depression of the gain of a fast conducting spinal sensorimotor path in humans. It was hypothesized that this gain control is mediated through a spinal circuit. In the first experiment, passive pedalling motion was rapidly initiated in eight able bodied subjects. Soleus H-reflexes (used to reveal the gain of the short latency stretch reflex) were recorded over the first 250 ms after the movement started. Significant depression in H-reflex magnitude was observed by 50 ms after the onset of movement. On the basis of the timing, this gain attenuation was likely mediated through a spinal circuit. In a second experiment we tested chronic quadriplegics with clinically complete lesions of the spinal cord. Of five subjects tested, three expressed the reflex and all three showed significant inhibition with passive pedalling movement (mean depression was to 39% of controls). Both the rapid onset of the gain change (Expt. 1) and the presence of movement-induced inhibition in individuals with spinal lesions (Expt. 2) provide evidence that this component of human locomotor control is located in the spinal cord. The initiating source is probably somatosensory receptor discharge due to the movement.

Generalisability of sensory gating during passive movement of the legs.

Movement-related gating of somatosensory evoked potentials in the upper limb is restricted mainly to nerve stimulation supplying the moved limb segment. In the lower limb, this principle may not be followed. Tibial nerve (stimulation at the knee) somatosensory evoked potentials (SEPs) and soleus H reflexes exhibit quite similar patterns of modulation during movement. We hypothesised that movement-related gating of initial SEPs in the leg would be generalised from ipsilateral to contralateral leg movement and that such sensory gating would not be generalised to modalities with no functional relevance to the movement. Somatosensory, visual, and auditory evoked potentials (SEPs, VEPs, and AEPs) were recorded from scalp electrodes during unilateral passive movement. Short-latency tibial nerve SEPs, representing the first cortical components, and soleus H reflexes in both the moved leg and the stationary leg were attenuated compared to non-movement controls (p<0.05). Neither VEPs nor middle latency AEPs were modulated (p>0.05). We conclude that sensory gating occurs during contralateral movement. This gating is absent in other sensory modalities with no apparent functional relationship to the imposed movement.

Long-lasting conditioning of the human soleus H reflex following quadriceps tendon tap.

Percussion of the quadriceps tendon was used to test the hypothesis that knee extensor muscle spindle discharge initiates down-regulation of the gain of the soleus H reflex. Seven subjects participated. Soleus H reflex magnitude was observed for up to 15 s, following conditioning tendon taps of 60 N or 80 N force and 10 ms duration, with the knee at 60 degrees or 90 degrees of flexion. The tap elicited quadriceps stretch reflexes in four subjects, with a mean latency of 42 ms. The major component of the conditioning of the soleus H reflex was significant attenuation of magnitude by 30-90% of controls, starting as early as 36 ms post-percussion and lasting as long as 3-8 s. The attenuation of reflex magnitude was evident, whichever combination of duration and force of tap was used. Preceding and/or following this inhibition, there was mild facilitation. Static stretch of quadriceps also significantly reduced soleus H reflex magnitude. These results support the spindle receptor origin for the gain attenuation seen during movement. The time course of the gain attenuation suggests a spinal route, by which the spindle discharge of the heteronymous extensor muscles initiates presynaptic inhibition of transmission through the reflex pathway.

Long-lasting inhibition of the human soleus H reflex pathway after passive movement.

Human soleus H reflexes are attenuated during passive pedalling movements. This depression occurs within 70 ms of movement onset. We hypothesized that the reflex gain would return to control values with a similar brevity following movement. However, H reflexes sampled following a slow (10 rpm) passive pedalling movement of a single leg remained below control values for the duration of a 200 ms collection period, for all four pedal positions tested. The extent of the attenuation after movement was position dependent in a manner similar to that observed during movement. This position effect was more precisely defined by sampling reflexes 200 ms post-movement at 10 pedal crank positions. Also, the full course of reflex recovery was investigated by sampling up to 8 s post-movement at four pedal positions. Reflex gain remained reduced 1-4 s post-movement, in a position dependent manner. There was a subsequent facilitation of the reflex. Thus, following a locomotor-like movement there is sustained attenuation of the soleus H reflex. The early post-movement period is likely the continued expression of movement-induced reflex inhibition while the later period may arise from descending influences consequent to the termination of movement. Presynaptic inhibition is implicated, as reflexes still showed the gain modulation when sampled while soleus was tonically contracted, both following and during the passive movement.