William Richard Staines

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.

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.

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.

Cutaneous reflexes of the human leg during passive movement

1 Four experiments tested the hypothesis that movement‐induced discharge of somatosensory receptors attenuates cutaneous reflexes in the human lower limb. In the first experiment, cutaneous reflexes were evoked in the isometrically contracting tibialis anterior muscle (TA) by a train of stimuli to the tibial nerve at the ankle. The constancy of stimulus amplitudes was indirectly verified by monitoring M waves elicited in the abductor hallucis muscle. There was a small increase in the reflex excitation (early latency, EL) during passive cycling movement of the leg compared with when the leg was stationary, a result opposite to that hypothesized. There was no significant effect on the magnitude of the subsequent inhibitory reflex component (middle latency, ML), even with increased rate of movement, or on the latency of any of the reflex components. 2 In the second experiment, the two reflex components (EL and ML) elicited in TA at four positions in the movement cycle were compared with corresponding reflexes elicited with the limb stationary at those positions. Despite the markedly different degree of stretch of the leg muscles, movement phase exerted no statistically significant effect on EL or ML reflex magnitudes. 3 In the third experiment, taps to the quadriceps tendon, to elicit muscle spindle discharge, had no effect on the magnitude of ML in TA muscle. The conditioning attenuated EL magnitude for the first 110 ms. Tendon tap to the skin over the tibia revealed similar attenuation of EL. 4 The sural nerve was stimulated at the ankle in the fourth experiment. TA EMG reflex excitatory and inhibitory responses still showed no significant attenuation with passive movement. Initial somatosensory evoked potentials (SEPs), measured from scalp electrodes, were attenuated by movement. 5 The results indicate that there is separate control of transmission in Ia and cutaneous pathways during leg movement. This suggests that modulation of the cutaneous reflex during locomotion is not the result of inhibition arising from motion‐related sensory receptor discharge.

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.

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.

Movement-induced gain modulation of somatosensory potentials and soleus H-reflexes evoked from the leg II. Correlation with rate of stretch of extensor muscles of the leg

Abstract Attenuation of initial somatosensory evoked potential (SEP) gain becomes more pronounced with increased rates of movement. Manipulation of the range of movement also might alter the SEP gain. It could alter joint receptor discharge; it should alter the discharge of muscle stretch receptors. We hypothesized that: (1) SEP gain reduction correlates with both the range and the rate of movement, and (2) manipulation of range and rate of movement to achieve similar estimated rates of stretch of a leg extensor muscle group (the vasti) results in similar decreases in SEP gain. SEPs from Cz’, referenced to Fpz’ (2 cm caudal to Cz and Fpz, respectively, according to the International 10–20 System), along with soleus H-reflexes were elicited by electrical stimulation of the tibial nerve at the popliteal fossa. Stable magnitudes of small M-waves indicated stability of stimulation. A modified cycle ergometer with an adjustable pedal crank and electric motor was used to passively rotate the right leg over three ranges (producing estimated vasti stretch of 12, 24 and 48 mm) and four rates (0, 20, 40 and 80 rpm) of movement. Two experiments were conducted. Ranges and rates of pedalling movement were combined to produce two or three equivalent estimated rates of tissue stretch of the vasti muscles at each of 4, 16, 32 and 64 mm/s. Tibial nerve stimuli were delivered when the knee was moved through its most flexed position and the hip was nearing its most flexed position. Means of SEP, H-reflex and M-wave magnitudes were tested for rate and range effects (ANOVA). A priori contrasts compared means produced by equivalent estimated rates of vasti stretch. Increasing the rate of movement significantly increased the attenuation of SEP and H-reflex gain (P<0.05). Increasing the range of movement also significantly increased these gain attenuations (P<0.05). Combining these to achieve equivalent rates of stretch, through different combinations of rate and range, resulted in equivalent depressions of SEP gain. H-reflex gains were similarly conditioned. These results suggest that muscle stretch receptors play a more important role than joint or cutaneous receptors in regulating SEP gain consequent to movement. We note that the present calculation only considers the knee extensors; however, the biomechanical model of stretch applies also to receptors in the hip extensors. This paper and the companion one show that primary factors in the kinaesthetic components of the movement regulate activity-induced gain attenuation of SEPs.

Modulation of H reflexes in human tibialis anterior muscle with passive movement

Significant movement-induced gain changes in H reflexes have been observed in soleus muscle following passive movement of the lower limb. Hypotheses from these concepts were tested on magnitudes of H reflexes in tonically contracted tibialis anterior. From eleven subjects at rates of 20 and 60 r.p.m. passive leg movement, statistically significant attenuation from controls and phasic modulation occurred. The results make more general the conclusions from soleus H reflexes. However, the functional effect should be much smaller, as tibialis anterior H reflexes are smaller compared to those in soleus.