Arthur Prochazka

Human H-reflexes are smaller in difficult beam walking than in normal treadmill walking

SummaryHoffmann (H) reflexes were elicited from the soleus (SOL) muscle while subjects walked on a treadmill and on a narrow beam (3.5 cm wide, raised 34 cm from the floor). The speed of walking on the treadmill was selected for each subject to match the background activation level of their SOL muscle during beam walking. The normal reciprocal activation pattern of the tibialis anterior and SOL muscles in treadmill walking was replaced by a pattern dominated by co-contraction on the beam. In addition, the step cycle duration was more variable and the time spent in the swing phase was reduced on the beam. The H-reflexes were highly modulated in both tasks, the amplitude being high in the stance phase and low in the swing phase. The H-reflex amplitude was on average 40% lower during beam walking than treadmill walking. The relationship between the H-reflex amplitude and the SOL EMG level was quantified by a regression line relating the two variables. The slope of this line was on average 41% lower in beam walking than treadmill walking. The lower H-reflex gain observed in this study and the high level of fusimotor drive observed in cats performing similar tasks suggest that the two mechanisms which control the excitability of this reflex pathway (i.e. fusimotor action and control of transmission at the muscle spindle to motoneuron synapse) may be controlled independently.

Voluntary and reflex control of human back muscles during induced pain

1 Back pain is known to change motor patterns of the trunk. The purpose of this study was to examine the motor output of the erector spinae (ES) muscles during pain in the lumbar region. First, their voluntary activation was assessed during flexion and re‐extension of the trunk. Second, effects of cutaneous and muscle pain on the ES stretch reflex were measured, since increased stretch reflex gain has been suggested to underlie increased muscle tone in painful muscles. 2 The trunk movement and electromyographical (EMG) signals from the right and left ES during pain were compared with values before pain. Controlled muscle pain was induced by infusion of 5% saline into the right lumbar ES. Cutaneous pain was elicited by mechanical or electrical stimulation of the dorsal lumbar skin. The stretch reflex was evoked by rapidly indenting the right lumbar ES with a servo‐motor prodder. 3 The results from the voluntary task show that muscle pain decreased the modulation depth of ES EMG activity. This pattern was associated with a decreased range and velocity of motion of the painful body segment, which would normally serve to avoid further injury. Interestingly, when subjects overcame this guarding tendency and made exactly the same movements during pain as before pain, the EMG modulation depth was still reduced. The results seem to reconcile the controversy of previous studies, in which both hyper‐ and hypoactivity of back muscles in pain have been reported. 4 In the tapped muscle, the EMG response consisted of two peaks (latency 19.3 ± 2.1 and 44.6 ± 2.5 ms, respectively) followed by a trough. On the contralateral side the first response was a trough (26.2 ± 3.2 ms) while the second (46.4 ± 4.3 ms) was a peak, similar to the second peak on the tapped side. Cutaneous pain had no effect on the short‐latency response but significantly increased the second response on the tapped side. Surprisingly, deep muscle pain had no effect on the stretch reflex. A short‐latency reciprocal inhibition exists between the right and left human ES. 5 It is concluded that deep back pain does not influence the stretch reflexes in the back muscles but modulates the voluntary activation of these muscles.

Movement illusions evoked by ensemble cutaneous input from the dorsum of the human hand.

1. In this study we tested the hypothesis that ensemble activity in human cutaneous sensory afferents evoked by the stretching of skin over and around the finger joints contributes to the conscious perception of movement of the fingers. 2. In nineteen normal adults, ensembles of cutaneous afferents were activated either by electrical stimulation, delivered through an array of electrodes on the dorsum of the hand and fingers, or by mechanical stretching of the skin over and around the joints. The stretching was applied through an array of threads stuck to the skin, in such a way as to avoid or minimize moving the underlying joints and to avoid applying pressure to underlying tendons and ligaments. Perceived movements were mimicked by voluntary movements of the fingers of the contralateral hand. 3. By way of comparison, kinaesthetic illusions were also evoked by activation of muscle receptors by vibration. 4. Illusions of movement were elicited with each type of stimulus. Electrical stimulation of skin afferents caused clear illusory movements in six out of seventeen subjects (35%), and borderline movement illusions in three out of the same seventeen subjects (total 9/17, 53%). Various other localized skin sensations were also reported. Skin stretch evoked movement illusions in eleven out of nineteen of subjects (58%). In all subjects who received both cutaneous stimuli, twelve out of seventeen (71%) reported some movement sensations with one or other of the stimulation techniques. Vibration tended to be the most reliable stimulus modality, eliciting illusory movements in fourteen out of sixteen subjects (88%). 5. Although the skin stretching technique did cause minute movements of nearby joints in several cases, these were monitored and shown in separate control experiments to be below perceptual threshold, and so the movement illusions could be safely attributed to the cutaneous afferent input evoked by skin stretch. 6. The results support the hypothesis that input from skin stretched during finger movement contributes to the conscious perception of the movement. Vibration‐evoked muscle afferent input tended to be more reliable than the skin input in producing kinaesthetic illusions, though comparisons of the relative efficacy of the three techniques must be made with caution.

Muscle spindle discharge in normal and obstructed movements.

1. The discharge activity of muscle spindle endings located in tail and hind limb muscles was recorded during voluntary movements in the cat. 2. During active shortening of the receptor‐bearing muscles, both primary and secondary endings tended to fall silent. This was more pronounced, the higher the rate of muscle shortening. We suggest that in unobstructed movements in which muscle velocities exceed 0.2 resting lengths per second (lr/sec), the firing patterns of spindle afferents are dominated by their responses to the length variations. At velocities lower than 0.2 lr/sec, fusimotor action may predominate. 3. When active muscle shortening was unexpectedly halted, both primary and secondary endings resumed firing, but the increases in discharge rate were not as abrupt as might have been expected had there been strong co‐activation of fusimotor and skeletomotor neurones. Rather, for the types of movements studied, fusimotor action appears to have been quite modest.

Ia afferent activity during a variety of voluntary movements in the cat.

1. Implanted dorsal root electrodes were used to record discharge trains of single spindle primary afferents (Ias) of the cats hind limb during different types of movement.

Models of ensemble firing of muscle spindle afferents recorded during normal locomotion in cats

1 The aim of this work was to compare the ability of several mathematical models to predict the firing characteristics of muscle spindle primary afferents recorded chronically during normal stepping in cats. 2 Ensemble firing profiles of nine hamstring spindle primary (presumed group Ia) afferents were compiled from stored data from 132 step cycles. Three sets of profiles corresponding to slow, medium and fast steps were generated by averaging groups of step cycles aligned to peak muscle length in each cycle. 3 Five models obtained from the literature were compared. Each of these models was used to predict the spindle firing profiles from the averaged muscle length signals. The models were also used in the reverse direction, namely to predict muscle length from the firing profiles. A sixth model incorporating some key aspects of the other models was also included in the comparisons. 4 Five of the models predicted spindle firing well, with root mean square (r.m.s.) errors lower than 14% of the modulation depth of the target profiles. The key variable in achieving good predictions was muscle velocity, the best fits being obtained with power‐law functions of velocity, with an exponent of 0.5 or 0.6 (i.e. spindle firing rate is approximately proportional to the square root of muscle velocity). The fits were slightly improved by adding small components of EMG signal to mimic fusimotor action linked to muscle activation. The modest relative size of EMG‐linked fusimotor action may be related to the fact that hamstring muscles are not strongly recruited in stepping. 5 Length was predicted very accurately from firing profiles with the inverse of the above models, indicating that the nervous system could in principle process spindle firing in a relatively simple way to give accurate information on muscle length. 6 The responses of the models to standard ramp‐and‐hold displacements at 10 mm s−1 were also studied (i.e. velocities that were an order of magnitude lower than that during stepping). In these cases components of spindle primary response related to length as well as velocity were needed for good fits. Because these length‐related components detracted from rather than improved predictions of the step cycle data, an attenuation of length dependence at high muscle velocities emerged as a possibility. 7 We conclude that in this study we have identified models and parameters that may be used to predict spindle afferent firing from the time course of muscle length in the cat step cycle.

Ensemble firing of muscle afferents recorded during normal locomotion in cats

1 The main purpose of this study was to collate population data on the firing characteristics of muscle afferents recorded chronically during normal stepping in cats. 2 Ensemble firing profiles of forty‐seven muscle spindle and tendon organ afferents were compiled from stored data. The relationships between the firing profiles and the displacement and force signals were analysed with the help of mathematical models of the response characteristics of spindle primary and secondary afferents and tendon organs. 3 Whereas the firing of hamstring spindle afferents could be predicted with reasonable accuracy from the length and velocity signals alone, the firing profiles of triceps surae spindle afferents deviated from the predicted profiles, particularly during electromyogram (EMG) activity. This indicated that the components of fusimotor action linked to extrafusal muscle activity were significant in triceps surae, possibly because this muscle is more strongly recruited in the cat step cycle. 4 From the limited data available, it was not possible to identify the ‘best’ or most general mathematical function to predict spindle secondary firing. In the two triceps surae spindle secondary units studied, firing was well predicted by using the simplest possible model, rate proportional to displacement, whereas in the hamstring spindle secondary data, a more complex linear transfer function was needed. The results of modelling the spindle secondary data were consistent with a modest amount of phasic, static fusimotor action linked to EMG activity. 5 The averaged ensemble of tendon organ afferent activity from the triceps surae gave predictions of whole‐muscle force that agreed well with separate triceps force measurements in normal cat locomotion. This supports the idea that ensembles of tendon organ afferents signal whole‐muscle force.   Our overall conclusion is that to a first approximation, large muscle afferents in the cat hindlimb signal muscle velocity, muscle length and muscle force, at least in movements of the speed and amplitude seen in locomotion.

What do reflex and voluntary mean? Modern views on an ancient debate

Abstract. Are the words reflex and voluntary useful scientific concepts, or are they prescientific terms that should be discarded? Physiologists use these words routinely in their publications, in laboratory experiments and, indeed, like most lay people, in their daily lives. The tacit assumption is that we all know, more or less, what they mean. However, the issue has a rich history of philosophical and scientific debate; and, as this article demonstrates, present-day researchers still cannot reach a consensus on the meaning of the words and on whether it is possible to draw a scientific distinction between them. The five authors present five quite different analyses. In broad terms, they split into two camps: those who equate voluntary behaviours with consciousness and suppressibility and those who view all behaviours as sensorimotor interactions, the complexity of which determines whether they are reflexive or voluntary. According to the first view, most movements of daily life are neither purely reflex nor purely voluntary. They fall into the middle ground of automatic motor programs. According to the second view, as neuroscience advances the class of reflex behaviours will grow and the class of voluntary behaviours will shrink.

Contribution of stretch reflexes to locomotor control: a modeling study

Abstract.It is known that the springlike properties of muscles provide automatic load compensation during weight bearing. How crucial is sensory control of the motor output given these basic properties of the locomotor system? To address this question, a neuromuscular model was used to test two hypotheses. (1) Stretch reflexes are too weak and too delayed to contribute significantly to weight-bearing. (2) The important contributions of sensory input involve state-dependent processing. We constructed a two-legged planar locomotor model with 9 segments, driven by 12 musculotendon actuators with Hill-type force-velocity and monotonic force-length properties. Electromyographic (EMG) profiles of the simulated muscle groups during slow level walking served as actuator activation functions. Spindle Ia and tendon organ Ib sensory inputs were represented by transfer functions with a latency of 35 ms, contributing 30% to the net EMG profile and gated to be active only when the receptor-bearing muscles were contracting. Locomotor stability was assessed by parametric variations of actuator maximum forces during locomotion in open-loop (“deafferented”) trials and in trials with feedback control based on either sensory-evoked stretch reflexes or finite-state rules. We arrived at the following conclusions. (1) In the absence of sensory control, the intrinsic stiffness of limb muscles driven by a stereotyped rhythmical pattern can produce surprisingly stable gait. (2) When the level of central activity is low, the contribution of stretch reflexes to load compensation can be crucial. However, when central activity provides adequate load compensation, the contribution of stretch reflexes is less significant. (3) Finite-state control can greatly extend the adaptive capability of the locomotor system.

Flexible fusimotor control of muscle spindle feedback during a variety of natural movements.

A refined version of an experimental iterative simulation method is described, which was used to infer, from chronic spindle afferent recordings, type and time course of static and dynamic fusimotor activation during a variety of voluntary movements. When used to estimate overall fusimotor drive (without distinction between static and dynamic action) the method provides unique solutions. However, when generating independent gamma s and gamma d activation profiles, the solutions no longer are strictly unique. Yet the boundary conditions imposed by the type specific characteristics of gamma-action nevertheless permit detection of powerful activation, especially of dynamic efferents. Extending the finding of selective dynamic fusimotor activation during unpredictably imposed and resisted stretches, evidence for powerful, often transient activation of dynamic efferents has now been obtained for three additional motor paradigms. First, initiation of walking was accompanied by mixed fusimotor action. Static drive was stepped up and then maintained, whereas dynamic drive declined after an initial abrupt peak. Second, corrective balancing on a narrow walk beam was characterized by largely maintained static background drive, whilst dynamic activation profiles often exhibited powerful surges or transients, when the animal crouched to regain balance. These preceded subsequent EMG bursts during the stretch phase of crouching by about 300 ms. Third, preparation for landing from rapid lowering featured prominent and possibly selective activation of dynamic fusimotor neurones, which peaked while the animal was in mid-air and declined upon landing, and which preceded the sharp onset of EMG after landing by several hundred milliseconds. In all cases the fusimotor activation profiles were unrelated to the parent muscle EMG and difficult to reconcile with the notion of alpha-gamma linkage or coactivation. These findings then clearly support the concept of flexible central control, particularly of dynamic gamma-motoneurones during certain motor tasks.