position in the standing position, and pressure on the soles of the feet due to the weight of the body. It is conceivable that

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1 4644 Journal of Physiology (1995), 488.1, pp Perception of movement at the human ankle: effects of leg position Kathryn M. Refshauge and Richard C. Fitzpatrick * Prince of Wales Medical Research Institute, High Street, Randwick, Sydney, NSW 2031, Australia 1. Recent studies show that subjects perceive smaller ankle movements when they are upright in the standing position than when they are seated. To examine this improvement, the ability to perceive ankle movements was tested in five positions of body, knee and ankle. Subjects reported the direction of slow ramp movements of the ankles. 2. The threshold for perceiving ankle movements was unchanged when only one ankle was moved rather than both together. When seated with the knees bent and ankles slightly plantarflexed, subjects perceived movements of 065 deg at 005 deg s-'. However, when upright or when seated with their knees and ankles in the standing position, subjects perceived movements that were one-third of this size. 3. These findings show that the knee and ankle positions, rather than being upright, explain the better performance in the standing position. During standing, knee extension and ankle dorsiflexion stretch the calf muscles. Thus, enhanced input from intramuscular stretch receptors appears responsible for the better performance. Thresholds for perceiving movement have long been studied because they provide a measure of sensory acuity. At the ankle, the ability to detect small movements is important to maintain stable standing. Nevertheless, for the past century the ability to perceive ankle movements has been measured while subjects were seated (Goldscheider, 1889; Gurfinkel, Lipshits & Popov, 1979; Clark, Burgess, Chapin & Lipscomb, 1985). Typically, subjects can perceive movements imposed on the ankle joint as small as 1 deg at 0 1 deg s-' (Refshauge, Chan, Taylor & McCloskey, 1995). However, in a recent study, movements one-fifth of this could be perceived when subjects were upright (Fitzpatrick & McCloskey, 1994). This improved performance when upright was not the result of muscle contraction during standing because subjects were held in an upright position so that they did not have to support the weight of the body. When subjects were supporting the weight of the body, as in normal standing, perceptual threshold was even further reduced. Several factors may account for the better proprioceptive performance at the ankle when subjects were upright. When seated, subjects were tested, usually at one ankle, with the knee bent and the ankle positioned in the middle of its range, and with minimal pressure on the sole of the foot. When upright, subjects had two ankles available for detection, their knees straight and ankles more dorsiflexed in the standing position, and pressure on the soles of the feet due to the weight of the body. It is conceivable that knee and ankle position may alter perceptual acuity by stretching the muscles that operate at the ankle joint. The present study was undertaken to identify the reasons for the better proprioceptive performance when upright than when seated. Proprioceptive acuity was measured at the ankle over a wide range of velocities that were selected to incorporate the relatively low velocities of normal body sway during standing. Acuity was measured in five leg positions to investigate reasons for the improved performance when upright. METHODS Ten healthy adults, aged between 21 and 42 years, participated in these simple non-invasive experiments. The authors were excluded and subjects were unaware of any experimental hypotheses and were given no information about their performance. The study was approved by the institution's human ethics committee. The experiments were designed to test the effect on perceptual acuity of: (i) the availability of proprioceptive inputs from either one or two legs; (ii) the position of the ankle in either the relative dorsiflexion of standing or the more plantarflexed position of relaxed sitting; (iii) the position of the knee in either extension as when standing or flexion while sitting; and (iv) the upright posture, one effect of which is to increase the pressure through the * To whom correspondence should be addressed. This manuscript was accepted as a Short Paper for rapid publication.

2 244 K. M. Refshauge and R. C. Fitzpatrick J Physiol feet and ankles. Performance was measured at velocities of 0 05, 0-25, 0 5 and 2-5 deg s-i. Set-up Five experimental conditions were tested. In each situation, movements of dorsiflexion and plantarflexion were imposed about the axis of the ankles using a linear servomotor under position feedback, and driven by a variable ramp generator. The test foot was supported on a metal plate against a heel rest and secured by a Velcro strap across the dorsum. The axis of rotation of the apparatus was aligned to be coaxial with the axis of rotation of the ankle joint (Soderberg, 1986). The leg and apparatus could not be seen by subjects, and auditory cues were eliminated by earmuffs. The five conditions (A-E) were as follows. A, sitting, one leg: subjects sat with the right foot resting on the footplate. The knee was in relaxed flexion (approximately 60 deg) and the ankle was in a relaxed position midway between full plantarflexion and full dorsiflexion - approximately 10 deg more plantarflexed than when standing (Fig. 1A). B, sitting, two legs: subjects sat with the knee and ankle in the position above, but with both feet on the footplate and separated by 20 cm (Fig. 1B). C, sitting, two legs, ankles dorsiflexed: subjects sat as in B but with the ankles in the standing position as measured for each subject (Fig. 1 C). D, sitting, two legs, ankles dorsiflexed, knees extended: subjects sat with the ankles in the standing position (C) and the knees straight. This is the position of the legs during standing except that the legs are horizontal and not loaded by the weight of the body. E, upright, two legs, knees and ankles in standing position, weight bearing: subjects were strapped to a rigid post to support them in the standing position. Although the weight of the body was applied through the feet and ankles, subjects did not contract the leg muscles to balance the body. This is the same leg configuration as shown in D but the subjects are upright. Detection levels in A and B were tested in one 3 h experimental session. Detection levels in C, D and E were tested in separate 1-5 h sessions. Frequent rests were allowed to prevent fatigue and to assist with concentration. Protocol Each movement began from an initial test position into either dorsiflexion or plantarflexion. The direction of the movements was randomized. Subjects were instructed to relax the leg muscles and to report the direction of any movement they perceived. To detect A Sitting, one leg D Sitting, ankles dorsiflexed, knees extended B Sitting E Upright, ankles dorsiflexed, knees extended C Sitting, ankles dorsiflexed Figure 1. Apparatus and positions to measure perception levels for ankle movements A, subjects were seated with the right knee flexed and the ankle in the middle of the plantarflexion-dorsiflexion range. B, subjects were seated with both legs in the position of A. C, subjects were seated with both knees flexed, and the ankles dorsiflexed into the standing position. D, subjects were seated with both ankles dorsiflexed and knees extended into the position of standing. E, subjects were supported upright with knees and ankles in the standing position. This is the same position as D but the weight of the body is supported through the feet and ankles. Note that, in all positions, the leg muscles were relaxed. The servomotor was used to apply small movements about the axis of the ankles of either plantarflexion or dorsiflexion.

3 J Phy8iol Perception of movement at the ankle 245 contractions of the leg muscles that might occur during the different conditions, electromyographic activity (EMG) was monitored from surface electrodes placed longitudinally over the right soleus muscle. To minimize guessing, subjects were asked to respond only when they could do so with certainty. Frequent reminders of these instructions were given to minimize incorrect reporting of direction (false positive responses) and responses in the absence of imposed movement. Care was taken not to give these reminders immediately after a false positive response. The effects of reaction time at higher velocities were overcome by allowing a 3 s period after the completion of the movement during which a response was accepted. For both flexion and extension, 70% detection levels were determined at each velocity by the method of Goldscheider (1889), which has been adopted by subsequent investigators. At each angular velocity, flexion and extension movements of a given amplitude were imposed on the test joint. The direction of the movement was varied in a random order, until ten flexion and ten extension movements had been imposed. Each displacement was held for 3 s before reset to the initial angle. The different velocities were tested in a random order. At each velocity, the 70% detection level was identified by adjusting the amplitude of displacement until subjects correctly reported seven out of ten movements. Data analysis Plantarflexion and dorsiflexion data were analysed separately using a Mann-Whitney rank sum test. These results did not reveal significant differences and subsequently all data were pooled. Comparisons were made between positions (A-E) and velocity using a two-way, repeated-measures ANOVA. Pairwise comparisons were made using Student-Newman-Keuls (SNK) post hoc analysis. RESULTS Subjects could perceive some movements before they could identify their direction, as reported in previous studies on both the upper and lower limbs (Laidlaw & Hamilton, 1937; Hall & McCloskey, 1983). Because event detection may depend on non-specific or non-proprioceptive cues, subjects were instructed to respond only when direction of movement was clear. Thus, by the criteria of this study, many imposed movements were 'undetected', although subjects might have been aware that some non-specific event had occurred. The low rate at which subjects named the wrong direction (< 4% false positives for any subject), confirms that subjects responded when they could do so with certainty. There was no significant difference in detection level between plantarflexion and dorsiflexion for any condition or velocity (Mann-Whitney rank sum, nineteen tests). Therefore, for subsequent analysis, plantarflexion and dorsiflexion data for each condition and velocity were combined. In all conditions, subjects perceived smaller displacements as the velocity of movement increased (ANOVA, F324 = 37 4, P < ), although there was a significant interaction between velocity and the experimental position (F9 72 = 7.5, P < 0O0001). Subjects' threshold for perceiving movements differed for the four experimental positions (conditions A, B, D and E, Fig. 1) that were initially tested (F324 = 22'6, P < ). When subjects were in the sitting positions with knees flexed and ankles dorsiflexed, performance was no better when both ankles were moved (condition B) than when the right ankle was moved (condition A; P > 0 05, SNK). When upright (E), or when sitting with the ankles dorsiflexed and the knees straight (D), subjects had their knees and ankles in the positions of normal standing, and there was no significant difference in performance between these conditions (P > 0 05, SNK). However, performance improved threefold when subjects had the legs in the standing position (D and E) compared with the sitting positions (A and B; P < 005, SNK). The slower movements examined here were equivalent to ankle movements during quiet standing. In the sitting positions, subjects could reliably detect movements of deg (condition A) and deg (B) at 0 05 deg s-', but in the standing positions they could detect movements as small as deg (D) and deg (E; means + S.E.M.; Fig. 2). To determine whether the improved performance in the standing Figure 2. Perception levels in the five knee and ankle positions Means + S.E.M. of angular displacements necessary for 70% correct detection of plantarflexion and dorsiflexion movements. The movements were applied at different velocities (log scale). Performance was best when the knee was extended and the ankle dorsiflexed (U while sitting and V while upright). Performance was worst when the knee was flexed and the ankle plantarflexed (A\ for one leg and A for two legs). With the knee flexed and the ankle dorsiflexed (A), performance was intermediate J Velocity (deg s-1)

4 246 K. M. Refshauge and R. C. Fitzpatrick J Phy8iol positions was due to the ankle dorsiflexion or to the knee extension, six subjects were tested with the knee flexed and the ankle dorsiflexed (condition C) at the three slower velocities. In this intermediate position, subjects could perceive smaller movements than when the ankles were plantarflexed (P < 0 05, SNK), but could not perceive movements as small as when the knee was extended (P < 0 05, SNK). At the slowest velocity of 0.05 deg s-', subjects could detect movements of 0 47 deg. DISCUSSION Comparison with previous studies of kinaesthetic thresholds at the ankle provides a convenient framework to discuss these results (Fig. 3). The present study shows that subjects' ability to perceive ankle movement is enhanced when they are upright in a standing position, confirming previous results obtained in sitting (Laidlaw & Hamilton, 1937; Gurfinkel et al. 1979; Refshauge et al. 1995) and upright (Fitzpatrick & McCloskey, 1994) subjects. Some studies have suggested significantly larger kinaesthetic thresholds for movement perception at the ankles (Goldscheider, 1889; Clark et al. 1985). Muscle contraction improves kinaesthetic performance (Taylor & McCloskey, 1992) and this could explain the lower perception threshold when subjects are standing (Gurfinkel et al. 1979; Fitzpatrick & McCloskey, 1994). However, in the present study, it is not muscle activity that explains the better performance when upright because subjects were not supporting a load, and because the EMG from soleus showed no contraction of the calf muscles, particularly when sitting with the knees straight, that could explain these findings. In addition, the better performance when upright is not due to a non-specific or vestibular facilitation of inputs related to ankle movement because subjects could perceive equally small movements when they were sitting with their legs in the 'standing position'. Sources of sensory information Cutaneous receptors in the soles of the feet and adjacent to the ankle, joint receptors in the capsule of the ankle and receptors in the leg muscles could potentially contribute to the perception of ankle movement. Cutaneous receptors In this study, when the body was supported upright and did not sway, correction forces were not produced by the leg muscles because they were not necessary. Consequently, the perpendicular force changes applied to the soles of the feet were negligible. However, in this position, ankle movement causes parallel shear forces to develop on the soles of the feet. For a typical subject, the shear force is approximately 250 g per 0-2 deg of ankle movement. Although this appears to be big, the large weight of the body means that it represents less than a 1% change in the background forces at receptor sites in the feet, less than the Weber fraction of 0 05 for weight discrimination (Ross & Brodie, 1987). Cutaneous receptors are, therefore, unlikely to account for subjects' better performance when upright than when sitting with the knees bent. Consistent with this interpretation, performance was no better when upright than when sitting with the knees extended. Joint receptors Most joint receptor firing occurs at the extremes of the range of joint movement and it is believed that, for most of '5 a) cz 0 a) a) A.A A...A n- A A -A. Clark et al o Refshauge et al 1995 Sitting o Laidlaw & Hamilton, 1937 V Gurfinkel et al 1979 O Goldscheider, 1889 Standing o Fitzpatrick & McCloskey, 1994 S v Gurfinkel et al 1979 * This paper Velocity (deg s-1) 5-0 Figure 3. Summary of reported detection thresholds at the ankle Data shown here are from previous comparable work (symbols) and the present study (small filled circles).

5 J Physiol Perception of movement at the ankle 247 the movement range, joint receptors probably play no more than a supportive or duplicative role to muscle receptors in kinaesthesia (Ferrell, Gandevia & McCloskey, 1987; Clark, Grigg & Chapin, 1989). In this study, the standing ('dorsiflexed') and sitting ('plantarflexed') positions are within the middle third of the total dorsiflexionplantarflexion range of movement. However, there are some human joint receptors whose firing rates are modulated within the mid-range (Burke, Gandevia & Macefield, 1988) and have been shown to evoke perceptions of joint movement (Macefield, Gandevia & Burke, 1991). In addition, a rise in intra-articular pressure may make these receptors more sensitive to movement (Ferrell et al. 1987). In the present study, intra-articular pressure would increase in the upright position because of the body weight, but this did not improve subjects' ability to perceive movement any more than positioning their knees and ankles identically when sitting (in Fig. 2, compare 'upright' (v) with 'sitting, knees straight, ankles dorsiflexed' (U)). Therefore, increased discharge from joint receptors can be discounted as an explanation for the improved proprioceptive performance in the upright position. Intramuscular receptors In the leg muscles, both Golgi tendon organs and muscle spindles are potential candidates to provide information about ankle movement. However, Golgi tendon organs are relatively insensitive to the passive external stretch that was used in this study: they respond more to the contraction of their associated motor units (Appenteng & Prochazka, 1984). Thus, it is more likely that subjects use signals from muscle spindles to perceive these passive movements (Goodwin, McCloskey & Matthews, 1972; Hall & McCloskey, 1983). In the cat soleus, muscle spindles respond to a stretch of 0002 % of muscle length (Matthews & Stein, 1969) and human spindles are probably as sensitive (Newsom Davis, 1975). The average length of human triceps surae fascicles is 38 mm and Achilles' tendon inserts 43 mm from the axis of the ankle (Yamaguchi, Sawa, Moran, Fessler & Winters, 1990) so that spindles in triceps surae could respond to movements of less than 0 01 deg. This spindle sensitivity is more than sufficient to account for the proprioceptive thresholds seen here in all experimental conditions. The population response of spindles is likely to be the effective sensory input, since firing of a single muscle spindle does not cause a perception of movement (Macefield et al. 1991). The total signal arising from the muscle spindle population will increase with passive stretch because more spindles will be recruited so that they have a background discharge that can be modulated by the movement. In this study, when the ankles were dorsiflexed, performance improved, and further improved when the knee was extended. The most consistent explanation for this finding is that these changes of knee and ankle positions apply successive stretch to triceps surae: knee extension stretches gastrocnemius whereas ankle dorsiflexion stretches both gastrocnemius and soleus. However, since there was no direction bias in movement detection, this explanation assumes that the spindle response from triceps surae more than compensates the reduced spindle discharge in antagonist muscle(s) (e.g. tibialis anterior) as stretch is reduced in these muscles. In the arm, an asymmetry of perception for flexion and extension has been described (Taylor & McCloskey, 1992), which suggests that such bias may be due to an asymmetry of agonist and antagonist muscle afferent discharge. Surprisingly, subjects' ability to perceive movement was not improved when two legs were available to provide information. This confirms previous findings of Gurfinkel et al. (1979), and suggests that information from each ankle does not converge to facilitate perception, but rather that information from each ankle is separately processed by perceptual centres to provide information about the ankles individually. APPENTENG, K. & PROCHAZKA, A. (1984). Tendon organ firing during active muscle lengthening in awake, normally behaving cats. Journal of Physiology 353, BURKE, D., GANDEVIA, S. C. & MACEFIELD, G. (1988). Responses to passive movement of receptors in joint, skin and muscle of the human hand. Journal of Physiology 402, CLARK, F. J., BURGESS, R. C., CHAPIN, J. 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6 248 K. M. Refshauge and R. C. Fitzpatrick J. Physiol LAIDLAW, R. WV. & HAMILTON, M. A. (1937). A study in thresholds of apperception of passive movement among normal control subjects. Bulletin of the NVeurological Institute of New York 6, MACEFIELD, G., GANDEVIA, S. C. & BURKE, D. (1991). Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. Journal of Physiology 429, MATTHEWS, P. B. C. & STEIN, R. B. (1969). The sensitivity of muscle spindle afferents to small sinusoidal changes in length. Journal of Physiology 200, NEwsoM DAvIs, J. (1975). The response to stretch of human intercostal muscle spindles studied in vitro. Journal of Physiology 249, REFSHAUGE, K. M., CHAN, R., TAYLOR, J. L. & MCCLOSKEY, D. I. (1995). Detection of movements imposed on human hip, knee, ankle and toe joints. Journal of Physiology 488, Ross, H. E. & BRODIE, E. E. (1987). Weber fractions for weight and mass as a function of stimulus intensity. Quarterly Journal of Experimental Psychology A 39, SODERBERG, G. L. (1986). Kinesiology. Application to Pathological Motion. Williams and Wilkins, Baltimore, MD, USA. TAYLOR, J. L. & AICCLOSKEY, D. I. (1992). Detection of slow movements imposed at the elbow during active flexion in man. Journal of Physiology 457, YAMAGUCHI, C. T., SAWA, A. G. U., AIORAN, D. W., FESSLER, M. J. & WINTERS, J. M. (1990). A survey of human musculotendon actuator parameters. In Alultiple Muscle Systems, ed. WINTERS, J. M. & Woo, L.-Y., pp Springer-Verlag, New York. Acknowledgements This study was supported by the National Health and Medical Research Council of Australia. The authors thank Professor D. I. McCloskey for his advice with this study. Received 20 MIay 1995; accepted 18 July 1995.