Medio-lateral balance adjustments preceding reflexive limb withdrawal are modified by postural demands.

We have recently observed medio-lateral balance adjustments (BA) preceding reflexive stepping elicited by noxious stimulation. While task specific modulation is evident for BA prior to voluntary leg movement, it is unclear whether rapid BA reactions (prior to 'reflexive' stepping) represent a generic response to evoked limb withdrawal or can be modified to suit task-conditions. This study was designed to establish whether the CNS is able to modify rapid onset latency BAs to match task conditions. Reflexive stepping was evoked by applying a noxious stimulus (50 ms stimulus train, 1 ms pulses, 300 Hz, 4 x perceptual threshold) to the plantar surface of the either the left or right foot. Task conditions were varied prior to stimulation by having subjects maintain one of three different static positions: (1) lean left (70% body weight (BW) on left), (2) neutral (50% BW both sides), (3) lean right (70% BW on right). BAs were denoted by centre-of-pressure (CoP) excursions towards the swing foot after the onset of noxious stimulation (average onset latency of 128 ms). There was a significant increase in frequency of occurrence and a significant increase in magnitude of CoP shift when the stimulation was applied to a loaded limb (leaning with 70% BW on the stimulated foot) as compared to an unloaded limb (30% BW). In addition, 78% of loaded trials featured steps taken with the unstimulated foot, which delayed removal of the stimulated foot. Collectively, the results indicate modifiability of the very rapid onset balance adjustments that precede the onset of limb withdrawal revealing complex control of balance exists even over very brief latencies.

Cortical representation of whole-body movement is modulated by proprioceptive discharge in humans.

Previous studies have revealed the influence of ongoing sensory discharge on modulating the central representation of muscle afferents from individual limbs. In the present study, we explored the potential for such modulatory influence on the afferent discharge arising from induced whole-body movement. Vestibular and somato-sensory inputs arise from such whole-body movement. The convergence of these two modalities is important in motor control, especially for the maintenance of postural stability. We hypothesised that transmission of proprioceptive and vestibular information to the cortex would be reduced as a result of muscle-spindle discharge in knee extensor muscles. Perturbation-evoked responses (PERs), recorded from central scalp electrodes (C3, CZ, C4), were evoked through rapid translations of subjects who were seated in a chair on a movable platform. PERs were recorded during passive linear translations alone and preceded by vibration of the patellar tendon. The PER was characterised by a slow, negative potential peaking at approximately 150 ms (N150) following displacement of the chair. The amplitude of the PER was reduced following vibration to 56% of the control. Such reduction of PERs was comparable to the attenuation of somatosensory evoked potentials and soleus H-reflex magnitudes from tibial-nerve stimulation. We conclude that muscle-spindle discharge in knee extensor muscles leads to gating of both of these afferent pathways. These results have potential implications to the understanding of the CNS control of stability during ongoing movement.

The gain of initial somatosensory evoked potentials alters with practice of an accurate motor task.

The gain of somatosensory afferent paths from the lower limb to the cerebral cortex was investigated during the acquisition of one target location during plantar flexion. Sensory gain was measured as the magnitude of somatosensory evoked potentials (SEPs) following electrical stimulation of a peripheral nerve in the lower limb, and was recorded from the scalp. We hypothesized gain attenuation of SEPs from sensory paths serving the limb segment responsible for target acquisition. SEP gain was studied as subjects plantar flexed about the anide to a target that was 15 degrees beyond the occurrence of a cutaneous stimulus (cue) to the lateral border of the foot. The "cue" was either fixed in one location or could appear at one of three positions in space. SEP gain was tested during practice and with task acquisition. Electroencephalographic (EEG) recordings were made of primary and secondary complexes of cortical SEPs from sural and tibial nerve stimulation, with 30-40 samples averaged per subject-condition. Electromyographic (EMG) records were made of soleus muscle H-reflexes and M-waves. Target acquisition was recorded as percent correct hits. The results showed significant attenuation in sural and tibial nerve primary SEPs with task acquisition when the cue was fixed or varied in movement space (P<0.05). Secondary SEPs from tibial nerve followed this pattern. Spinal H-reflexes only attenuated with movement per se. We conclude that the CNS preferentially reduces the cerebral inflow of sensory information once such a motor task has been successfully acquired.

Vibration-induced inhibition of the early components of the tibial nerve somatosensory evoked potential is mediated at a spinal synapse.

OBJECTIVES: To investigate whether afferent-induced suppression of cortical somatosensory evoked potentials (SEPs) occurs at a spinal site along the transmission route of afferent signals from the tibial nerve to the primary somatosensory cortex. METHODS: Evoked potentials were recorded at 4 points (sciatic nerve, L5, C1, and cortex) along the path of transmission following electrical stimulation of the tibial nerve in halothane-anesthetized cats. The amplitudes of evoked potentials sampled during vibration of quadriceps were compared to evoked potentials sampled without the vibration. RESULTS: The spinal SEP recorded at C1 and the cortical SEP were both substantially reduced by patellar tendon vibration. The L5 spinal SEP and the sciatic nerve potential were unaffected. Vibration of quadriceps did not influence the latency of the evoked potentials. CONCLUSIONS: These results indicate that afferent-induced suppression of the initial complex of the SEP can be mediated at a spinal synapse.

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.

Upper limb H reflexes and somatosensory evoked potentials modulated by movement.

In the human lower limb, the magnitudes of both Hoffmann (H) reflexes and primary somatosensory evoked potentials (SEPs) from scalp electrodes, are reduced by active and/or passive movement. We surmised that similar effects occur for the upper limb and specifically hypothesised that amplitudes of median nerve induced flexor carpii radialis H reflexes and cortical SEPs are reduced with passive movement about the wrist or elbow. The results showed (P<0. 05) that either movement significantly attenuated mean magnitudes of SEPs elicited from stimulation at elbow or wrist and that reflex magnitudes attenuated with wrist movement. Thus, the upper limb shows similar movement-induced modulation to the lower limb. These attenuations of fast conducting sensory paths consequent to movement per se, may be a basic level of motor control, initiated from muscle mechanoreceptor discharge. Upon this basic level, more complex modulations then may be laid as appropriate for the particular characteristics of active motor tasks.

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.

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.

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.

Preparatory balance adjustments precede withdrawal response to noxious stimulation in standing humans.

Self-initiated leg movement in standing humans is preceded by a medio-lateral preparatory balance adjustment (PBA); however, such preparatory balance control is often absent in reflex-like stepping responses evoked by whole-body instability. The presence or absence of the PBA may reflect a task-dependent modulation of the response serving to preserve lateral stability (PBA present) or avoid delay in the lifting of the foot (PBA absent). To examine whether such task-dependent modulation can occur during more stereotypical limb movements, we examined spinally-mediated withdrawal responses evoked by noxious stimulation of the foot. Results showed that rapid limb withdrawal was preceded by a large PBA when subjects were standing but not when they were supine. The PBA caused limb withdrawal to the noxious stimulation to be delayed. However, the onset of the PBA in the standing trials was equivalent in timing to the onset latency of the classic withdrawal responses recorded during the supine trials. Evidence of a preparatory balance adjustment evoked, in advance of a delayed withdrawal response, at very rapid latencies (underlying muscle activation at 70-120 ms) may raise new questions about the neural mechanisms underlying the co-ordination of balance and 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.

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.

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.

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.

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

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.

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.

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.

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.

Modulation of cerebral somatosensory evoked potentials arising from tibial and sural nerve stimulation during rhythmic active and passive movements of the human lower limb.

The magnitudes of cerebral somatosensory evoked potentials (SEPs), following stimulation of cutaneous or muscle afferents in the upper limb, are reduced during active and passive movements of the fingers. The generalizability of such a movement effect was tested for lower limb events. We measured SEP magnitudes following activation of cutaneous (sural) and mixed (tibial) nerves during the flexion phase of active and passive rhythmic movements of the human lower limb. In eight volunteers, 150 SEPs per condition were recorded from Cz' referenced to Fpz'. Compared to stationary controls, both active and passive movements significantly depressed the early SEP components (P1-N1) [mean values, to 12.8%, 9.9% respectively for tibial nerve and to 29.6%, 25.6% for sural nerve stimulation, p < 0.05]. The attenuation was still observed when only one leg was moved and with stimulation at an earlier point in the flexion phase of movement. Visual fixation did not significantly affect P1-N1 amplitudes, compared to eyes closed. As previously shown, soleus H reflexes with stable M waves were significantly depressed during the movements (p < 0.05). The general construct may be that centripetal flow initiated from somatosensory receptors during limb movement leads to modulation of both spinal and cortical responses following large diameter cutaneous or muscle afferent activation.

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.

Mechanisms within the spinal cord are involved in the movement-induced attenuation of an H reflex in the dog.

1. H reflexes were elicited in the second interosseous muscle of the hindpaw of the anesthetized dog during passive rotation of the shank about the ipsilateral or contralateral knee. Reflexes sampled at four points in the cycle of movement were compared with stationary controls. For both the ipsilateral and contralateral limb manipulations, reflexes were significantly reduced (P < 0.05) across the cycle of movement. Position-related modulation of the reflex amplitude was not detected (P > 0.05) in either instance. 2. The experiments were then repeated after the spinal transection of each animal at the level of T13. Passive rotation about either the ipsilateral or contralateral knee significantly attenuated (P < 0.05) the H reflex across a cycle of movement in the spinal dog. There was little difference in the amount of inhibition produced by the movement between the intact and spinal animals. On average, the reflex was attenuated 29 +/- 2.4% (mean +/- SE) in the intact animals and 32 +/- 2.1% in the spinal animals. 3. It is concluded that passive rotation about the knee of either leg leads to suppression of the H reflex of the second interosseous muscle both in the ipsilateral, moving leg and the contralateral, stationary one. This reflex suppression occurs across the cycle of movement. The mediating circuitry lies within the spinal cord, caudal to T13.