Journal of Physiology (1992), 458. pp. 69-83 With 6 figures Printed in Great Britain

69

POSTURAL PROPRIOCEPTIVE REFLEXES IN STANDING HUMAN SUBJECTS: BANDWIDTH OF RESPONSE AND TRANSMISSION CHARACTERISTICS

BY RICHARD C. FITZPATRICK, ROBERT B. GORMAN, DAVID BURKE AND SIMON C. GANDEVIA From the Prince of Wales Medical Research Institute, University of New South Wales and the Department of Neurology, The Prince Henry and Prince of Wales Hospitals, Sydney 2036, Australia

(Received 15 October 1991) SUMMARY

1. This study investigated the reflex control of postural sway during human bipedal stance. The experiments were designed to: (i) find evidence for the operation of 'stretch reflex' pathways during quiet stance, (ii) determine the bandwidth of the reflex response, (iii) describe the reflex transmission characteristics in standing subjects, and (iv) assess the ability of subjects to make a task-dependent change in the reflex. 2. A continuous ranidom perturbation that did not threaten stability was applied at waist level to nine staiiding subjects. The effects of the perturbation on ankle torque, ankle movement and soleus electromyographic activity (EMG) were identified by cross-correlation. The bandwidth of the reflex response and the transmission characteristics of reflexes that respond to ankle movement were identified by spectral analysis. Changes in these reflex responses were investigated when subjects attempted to stand as still as possible, had their eyes closed, or balanced a load equivalent to their own body in a situation in which neither visual nor vestibular reflexes would be activated. 3. When standing, a reflex response coherent with the perturbation was seen in soleus EMG at frequencies up to 5 Hz, with mnaximal coherence at 1V0-2 0 Hz. Reflex gain increased with frequency, and there was a frequency-dependent phase advance of soleus EMG on ankle movement reaching 135 deg at 3 Hz. When attempting to minimize sway, subjects produced a more coherent reflex response and significantly increased reflex gain. 4. The response and transmission characteristics of the lower limb proprioceptive reflex in freely standing subjects were similar to those in subjects balancing a load at the ankle, a situation in which vestibular and visual inputs could not contribute. 5. It is concluded that reflex feedback related to ankle movement contributes significantly to maintaining stance, and that much of the reflex response originates from lower limb mechanoreceptors stimulated by ankle rotation. Although reflex gain may be relatively low during quiet stance it can be increased when necessary to maintain stability. MS 9817

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R. C. FITZPATRICK AND OTHERS INTRODUCTION

During human bipedal stance, body movements and external disturbances apply continuous perturbing torques at the ankles. If balance is to be maintained, those perturbations which might destabilize posture must be opposed by co-ordinated responses from leg muscles. Previous studies of human stance have generally used abrupt and often large disturbances of the standing posture to investigate these reflexes (Nashner, 1976, 1977; Bussel, Katz, Pierrot-Deseilligny, Bergego & Hayat, 1980; Diener, Dichgans, Bootz & Backer, 1984; Dietz, Quintern, Berger & Schenck, 1985; Dietz, Horstmann & Berger, 1989; Nardone, Giordano, Corra & Schieppati, 1990). Other studies have used electrical stimulation of peripheral nerves and measured H-reflex responses (Katz, Meunier & Pierrot-Deseilligny, 1988), or the effects of non-muscular afferent discharge on motoneuron excitability (Aniss, Diener, Hore, Burke & Gandevia, 1990). These studies have identified and measured the latencies of visual, vestibular and proprioceptive reflexes which may operate to maintain upright human stance. However, the large synchronized neural discharges evoked by these stimuli could reflect only those physiological mechanisms designed to prevent falling, rather than the operation of the motor control system responsible for quiet stance, and they do not describe the bandwidth within which postural reflexes operate. Using linear analysis techniques on non-linear biological systems may lead to errors of interpretation if they are used to predict responses to stimuli with different characteristics (Rack, 1981). In a non-linear system, a response to a large stimulus is not necessarily proportional to the response evoked by a smaller stimulus. Similarly, the responses to impulsive or sinusoidal disturbances may not reflect the responses to the continuous, random disturbances which are likely to prevail during quiet stance. Cross-correlation and frequency analysis have been used to measure the dynamic characteristics of the biceps-brachii stretch reflex (Neilson, 1972a). This technique avoids the use of impulse response analysis, permitting the use of a more physiological, continuous perturbation. Thus, the results obtained from linear analysis can be more reliably interpreted (Maki, 1986). Cross-correlation can isolate the response to a comparatively small perturbing stimulus from more prominent activity such that the normal reflex operation is not overridden by the need to use a large stimulus. Three functions in the frequency domain (coherence, gain and phase) are used to describe the correlated components of ankle movement as an input and soleus EMG as an output of the reflex pathways. The present study of standing subjects uses cross-correlation and frequency analysis, to identify in soleus, reflexes associated with ankle movements produced by a near-physiological, continuous perturbation. The results demonstrate reflex activity which stabilizes upright stance by responding to small, continuous postural disturbances, and show that these reflexes can be modified according to subject's volitional set. Furthermore, the results suggest that much of the reflex response originates from lower limb mechanoreceptors stimulated by ankle rotation.

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METHODS

Eleven healthy adults, including the authors, provided informed consent to the experimental procedures. They ranged in age from 22 to 46 years, and weighed between 57 and 89 kg. Experimental protocol. Each subject stood on a stable force platform, without shoes, and with feet separated by approximately 200 mm. A position-controlled linear servomotor (Servotron, Sydney) was attached through a weak spring (40 N m-l) to a firmly fitting belt worn around the Natural disturbance Experimental

disturbance

Torque-related

reflexes

+

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Ankle Ankle trque Body angle load

ISoleus

Muscle muscle force

-

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Angle-related reflexes

Soleus EMG

4k +

Motor

command Fig. 1. A closed-loop model of the information flow in the control of stance. Internal and external disturbances (which may include the experimental perturbation) produce torques which act at the ankles. The torque causes an ankle movement that is determined by the load properties at the ankles. Movement-related reflexes result in activation of the leg muscles, and so produce an ankle torque which counteracts the initial perturbing torque. It is also possible that these reflexes may respond to ankle torque (dashed line). An open-loop control involving a non-reflex motor command that acts directly on the leg muscles may also be active.

pelvis. The motor was controlled by a continuous random stimulus signal which had been filtered so that it had power at frequencies between 0-1 and 10 Hz. The perturbation was too small to threaten the subjects' stability, but was sufficiently large to increase the sway of their normal stance. This spring-body system would function as a low-pass filter with a frequency response affected by each subject's weight. Subjects stood for four experimental trials of 400 s duration, and rested in a seated position for at least 10 min between each. For each trial, they either had their eyes open or had their eyes shut and, for each of these cases were given instructions to either stand 'still' (i.e. minimize their sway) or stand 'relaxed' (i.e. disregard their sway). The sequence of these four tasks was randomized between subjects. Ankle angle, ankle torque, and the surface electromyogram (EMG) of soleus and tibialis anterior were recorded from the right leg. Three subjects were perturbed using a 'predictable' disturbance signal of constant amplitude but increasing or decreasing slowly and progressively in frequency, much as used by Brown, Rack & Ross (1982) and Evans, Fellows, Rack, Ross & Walters (1983) to impose sinusoidal movements to the thumb and ankle. A second series of similar experiments was performed to determine the response to the same perturbation if only lower limb proprioceptive information was available while subjects performed an equivalent task to standing. Subjects were supported in an upright position by a rigid post which prevented body sway and so eliminated vestibular stimulation (see Fitzpatrick, Taylor & McCloskey, 1992). In this position and with their eyes shut, they used their feet to balance a nearvertical load that was similar to the load of their body when standing freely. The balancing task required subjects to maintain a constant ankle angle. This load had an axis of rotation co-linear with the axis of the ankles. The load could therefore be regarded as an 'equivalent person' imposing

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R. C FITZPATRICK ANTD OTHERS

the same torque at the ankles as a subject's own body did when standing. The servomotor and spring were used to perturb the load while subjects attempted to hold it still. To assess the ability of subjects to produce a coherent voluntary response to the perturbing stimulus, three voluntary tracking experiments were performed. In the first task, subjects were asked to track the perturbation by swaying voluntarily when standing with eyes shut. Two tasks were performed on seated subjects to determine their ability to produce a coherent response to the same stimulus when they were not standing. Each subject sat in a chair with the knees within 10 deg of full extension. The right foot was placed on a plate that rotated freely about an axis colinear with the axis of the ankle. The plate was attached through a pivoted strain gauge to a large, near-vertical beam which provided the load. The load was chosen to apply a similar torque (10-15 N m) and angle-torque relationship (stiffness) to those at the ankle when standing. The servomotor, driven by the same random signal, was connected through a weak spring to perturb the beam while the subject balanced it. Each subject attempted to track the perturbation with the right leg. For the third tracking task, the left foot was placed on a foot plate that was attached to a stiff spring. Using the left foot, subjects attempted to track the perturbation that was applied to the right foot. For each tracking task, the coherence between the soleus EMG and the perturbing signal provided a measure of the subject's ability to produce a coherent voluntary response.

Three subjects stood 'still' with eyes shut for 400 s of unperturbed stance. These experiments provided control data for the perturbation. Data measurement. The platform on which subjects stood comprised four rigid cantilevered plates, each fitted with a set of strain gauges. Subjects stood with their heels on the posterior plates and forefeet on the anterior plates, with the feet placed in the same positions on the platforms for each experimental trial. The difference between the force signals from the right-anterior and right-posterior plates was recorded. This signal was linearly proportional to ankle torque for each subject. The torque signal had a noise level equivalent to < 005 N m, whereas the measured range of torque during an experiment was approximately 10 N m. When balancing the equivalent load, ankle torque was measured using a strain gauge that attached the rotating foot platforms to the load (see Fig. 1 in Fitzpatrick et al. 1992). The actual perturbing force was measured by a strain gauge that connected the servomotor to the spring. When standing, ankle angle was derived using a pair of linearized magnetometers; one attached over the subject's tibial tuberosity and the other attached to a rigid support. The resultant signal was proportional to the distance separating the magnetometers and therefore proportional to ankle angle. When balancing the equivalent load, the magnetometers were used to derive ankle angle from the angle of the load to the vertical. The magnetometer signal had a noise level equivalent to < 0001 rad, whereas the measured range of ankle rotation during an experiment was approximately 0 04 rad. EMG was recorded using surface electrodes placed 6-8 cm apart and oriented longitudinally over the right soleus and tibialis anterior. The EMG signals were filtered with a bandwidth of 100-10000 Hz, full-wave rectified, and then integrated with a decay time constant of 100 ms. The absolute values of the perturbing force, torque, angle and EMG were unnecessary for the analvsis technique. Care was taken to ensure that conditions remained constant between the different experimental trials for each subject. Data analysis. During the experimental trials the data signals were recorded on tape. The signals were played back off-line through identical bandpass filters (005-25 Hz). For computer analysis, an analog-to-digital interface sampled each signal at 50 Hz. Cross-correlation and spectral analysis were used to identify the reflex transmission properties (Jenkins & Watt, 1968). The power spectra of the measured variables (perturbing force, ankle torque, ankle angle. soleus EMG) and the correlated power (cross-power spectra) between the stimulus signal and these variables were calculated.The coherence, gain and phase functions between the stimulus signal and the measured variables were obtained from the power and cross-power spectra. At any given frequency, coherence is a measure of the strength of association between the two signals, and is defined as the squared correlation between the Fourier transforms of the signals. At any given frequency. gain is the input-output amplification between the coherent components of the signals. Phase is the shift in degrees between the coherenit components of the signals. A phase lag does not represent a time delay in signal transmission; however, a fixed transmission delay would cause a phase lag which increased with frequency. The power spectra and gain functions were expressed in arbitrary units, but the coherence function (C,) has a range of 0 < Cf < 1.

POSTUTRAL REFLEXES IN STANDING HUMANS

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A model of a feedback position control system which may operate when standing (Fig. 1) was the basis for an open-loop analysis of reflex transmission. The stimulus-to-EMG gain was divided by the stimulus-to-angle gain, to obtain an estimate of the open-loop gain of the reflex pathways that may respond to ankle movement. Similarly, the stimulus-to-angle phase was subtracted from the stimulus-to-EMG phase to obtain the open-loop phase function. This linear analysis technique was based on an information flow model adapted from the studies of Neilson (1972a), Houk & Rymer (1981), Rack (1981), and Maki (1986). For each subject, the reflex gain functions were normalized so that the average gain over 0-25-5-0 Hz for the combined standing trials was unity. For the balancing task, the reflex gain was separately normalized to an average of unity for each subject. For each experimental condition, an average gain function for all subjects was calculated from the normalized gain functions. The phase and coherence functions were averaged without normalizing. Geometric averages were calculated from the individual power spectra. The EMG power spectra and the gain and phase functions were corrected for the filtering effects of the EMG integrator. The transfer function of the integrator was determined empirically by passing EMG sequences through the integrator and analysing the input and output signals. Confidence limits. The duration of each sequence (400 s) was chosen to give a confidence level of 01 for spectral estimates and the coherence functions, based on a sampling rate of 50 Hz and spectral resolution of 0-25 Hz (Jenkins & Watt, 1968). RESULTS

A continuous random perturbation was applied to nine standing subjects in four experimental conditions: (i) standing 'still' with eyes open. (ii) standing 'still' with eyes shut, (iii) standing ' relaxed' with eyes open, (iv) standing 'relaxed' with eyes shut. A similar disturbance was applied as nine subjects (including seven of the above) balanced a load which was equivalent to their owAn body in a situation in which neither visual or vestibular afferent information could be used.

Perturbing stimulus The applied perturbation was small, with the largest peak-to-peak forces at the waist being approximately 200 g. It was not threatening to subjects' stability, and large postural reactions were not seen. To estimate the effect of the perturbation on ankle movement, ankle torque and soleus EMG, their power spectra during perturbed and unperturbed stance were compared for three subjects who stood 'still' with their eyes shut. In both situations, ankle movement and ankle torque showed a low-pass filter effect, with a pronounced attenuation above 2 0 Hz. The power spectrum of the perturbing signal had a similar profile (Fig. 2). Soleus was continuously active when subjects were standing freely and when they were being perturbed. During unperturbed stance, the EMG power was distributed relatively uniformly across the 025--50 Hz domain. From the power spectrum, it was estimated that ankle movement increased by an average of 35 % when the perturbation was applied, without a dominant resonant frequency. In contrast, the soleus EMG showed a non-uniform increase, with a peak of power at 1P0-2 0 Hz. Tibialis aniterior EMG remained silent (i.e. less than that which could be attributed to field spread from soleus) during the standing and balancing experimental trials, a finding which confirms that the perturbation was insufficient to jeopardize balance.

R. C. FITZPATRICK AND OTHERS

74

Reflex and voluntary responses Reflexes when standing With each experimental condition in the standing subjects, the perturbation produced significant coherent responses in ankle torque, ankle movement and soleus A

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Frequency (Hz) Frequency (Hz) 2. The means of the from three subjects for perturbed Fig. power spectra (arbitrary units) and unperturbed stance are shown in A. Filled symbols represent perturbed stance and unfilled symbols, unperturbed. The soleus EMG power spectra show little attenuation at the higher frequencies, whereas the ankle movement power is predominantly below I Hz. B shows the difference in power between the perturbed and unperturbed conditions. These are shown with the power spectrum of the perturbation (labelled 'input'). The difference in ankle movement is similar to the power spectrum of unperturbed stance (A ). This was achieved by having an input spectrum with similar power content. In contrast, the EMG response is greatest at frequencies above I Hz.

EMG from 0-25 to 5 0 Hz, with the highest coherences at 1 0-2 0 Hz (Fig. 3A). These coherence functions describe the proportion of soleus EMG that is linearly correlated with the disturbance signal at each frequency, and are analogous to the square of the correlation coefficient. They provide a measure of the size of the reflex response. For the coherences calculated here (data sampled at 50 Hz for 400 s, with a spectral resolution of 0 u25 Hz) the normalized standard error for each spectral estimate and coherence function is 0w10. For each subject coherence was greater when standing Bstill' than when standing 'relaxed' in both the eyer-open and eyes-shut conditions at Hz, P

Postural proprioceptive reflexes in standing human subjects: bandwidth of response and transmission characteristics.

1. This study investigated the reflex control of postural sway during human bipedal stance. The experiments were designed to: (i) find evidence for th...
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