J.D. Brooke

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.

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)

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.

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.

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.

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.

Movement-induced gain modulation of somatosensory potentials and soleus H-reflexes evoked from the leg. I. Kinaesthetic task demands

Abstract Movement-related gating of cerebral somatosensory evoked potentials (SEPs) occurs during active and passive movements of both the upper and the lower limbs. The general hypothesis was tested that the brain participates in setting the gain of the ascending path from somatosensory receptors of the human leg to the somatosensory cortex. In experiment 1, SEPs from Cz’ and soleus H-reflexes were evoked by electrical stimulation of the tibial nerve in the popliteal fossa during passive movement about the right ankle. Early SEPs and H-reflexes sampled during simple passive movement were significantly attenuated when compared with stationary controls (P<0.05). The additional requirement of tracking the passive ankle movement with the other foot led to a significant relative facilitation of mean SEP, but not H-reflex amplitude, compared with means from passive movement alone (P<0.05). In experiment 2, SEPs were evoked in the active (tracking) leg during a forewarned reaction-time task. Subjects were required to move in a preferred direction or to track the passive movement of their right foot with their left. Significant attenuation of early SEP components occurred 100 ms prior to EMG onset (P<0.05), with no apparent effect due to tracking. In the 3rd experiment, SEPs and H-reflexes were evoked in the passively moved leg (the target for active movement of the left leg) during the same forewarned reaction-time task. During the warning period, SEPs were significantly attenuated compared with stationary controls for non-tracking movements, but not for movements involving tracking (P<0.05). It is concluded that centrifugal factors are important in modulating SEP gain required by the kinaesthetic demands of the task.

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.

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.

Locomotor-Like Rotation of Either Hip or Knee Inhibits Soleus H Reflexes in Humans

Human soleus H reflexes are depressed with passive movement of the leg. We investigated the limb segment origin of this inhibition. In the first experiment, H reflexes were evoked in four subjects during (1) passive pedaling movement of the test leg at 60 rpm; (2 and 3) pedaling-like flexion and extension of the hip and the knee of the test leg separately; and (4) stationary controls. In the second experiment, with the test leg stationary, the same series of movements occurred in the opposite leg. Rotation of the hip or the knee of the test leg significantly reduced mean reflex amplitudes (p < 0.01) to levels similar to those for whole-leg movement (mean H reflexes: stationary, 71%; test leg pedaling movement, 10%; knee rotation, 15%; hip rotation, 13% [all data are given as percentages of Mmax]). The angle of the stationary joint did not significantly affect the results. Rotation of the contralateral hip significantly reduced mean reflex magnitudes. Rotation of the contralateral knee had a similar effect in three of the four subjects. We infer that a delimited field of receptors induces the movement conditioning of both the ipsilateral and contralateral spinal paths. It appears that somatosensory receptor discharge from movement of the hip or knee of either leg induces inhibition as the foundation for the modulation of H reflexes observed during human movement.