mainly due to a disproportionate reduction in the angular motion about the ankles

Transcription

1 Journal of Phy8iology (1993), 469, pp With 9 figure Printed in areat Britain EFFECT OF VISION AND STANCE WIDTH ON HUMAN BODY MOTION WHEN STANDING: IMPLICATIONS FOR AFFERENT CONTROL OF LATERAL SWAY BY B. L. DAY, M. J. STEIGER, P. D. THOMPSON AND C. D. MARSDEN From the MRC Human Movement and Balance Unit, Institute of Neurology and National Hospital for Neurology and Neurosurgery, Queen Square, London WCIN 3BG (Received 12 November 1992) SUMMARY 1. Measurements of human upright body movements in three dimensions have been made on thirty-five male subjects attempting to stand still with various stance widths and with eyes closed or open. Body motion was inferred from movements of eight markers fixed to specific sites on the body from the shoulders to the ankles. Motion of these markers was recorded together with motion of the point of application of the resultant of the ground reaction forces (centre of pressure). 2. The speed of the body (average from eight sites) was increased by closing the eyes or narrowing the stance width and there was an interaction between these two factors such that vision reduced body speed more effectively when the feet were closer together. Similar relationships were found for components of velocity both in the frontal and sagittal planes although stance width exerted a much greater influence on the lateral velocity component. 3. Fluctuations in position of the body were also increased by eye closure or narrowing of stance width. Again, the effect of stance width was more potent for lateral than for anteroposterior movements. In contrast to the velocity measurements, there was no interaction between vision and stance width. 4. There was a progressive increase in the amplitude of position and velocity fluctuations from markers placed higher on the body. The fluctuations in the position of the centre of pressure were similar in magnitude to those of the markers placed near the hip. The fluctuations in velocity of centre of pressure, however, were greater than of any site on the body. 5. Analysis of the amplitude of angular motion between adjacent straight line segments joining the markers suggests that the inverted pendulum model of body sway is incomplete. Motion about the ankle joint was dominant only for lateral movement in the frontal plane with narrow stance widths (< 8 cm). For all other conditions most angular motion occurred between the trunk and leg. 6. The large reduction in lateral body motion with increasing stance width was mainly due to a disproportionate reduction in the angular motion about the ankles and feet. A mathematical model of the skeletal structure has been constructed which offers some explanation for this specific reduction in joint motion. MS 1898

2 480 B. L. DAY AND OTHERS 7. The model demonstrates that when the knees are locked the joints of the ankles and hips become coupled together so that movement of one is accompanied by movement of the others. The strength of this coupling increases with stance width. The stiffness of the legs-pelvic structure is therefore passively increased by increasing stance width. 8. Coupling of the hips and ankles also predicts an increase in proprioceptive sensitivity to lateral motion about the ankles with increasing stance width, a factor which may contribute to the observed reduction in lateral motion. At the same time the model predicts that information from receptors in the head (visual and vestibular) become less sensitive in the detection of lateral motion about the ankles with increasing stance width. This may explain why vision was less effective in reducing lateral velocity of the body with greater stance widths. INTRODUCTION Even when attempting to stand still the upright human body continues to move. For a healthy person these residual movements are usually not a problem since the magnitude of body motion that remains is too small to threaten equilibrium; the vertical projection of the body's centre of mass can be readily maintained within the area of support bounded by the outer edges of the feet. However, difficulty may be experienced by patients with central nervous system damage when attempting to stand upright because of excessive sway. The pattern of residual body motion may be quite different for patients with lesions at different sites. For example, patients with alcoholic cerebellar degeneration predominantly affecting the anterior lobe of the cerebellum have been reported to exhibit pronounced anteroposterior body movements at around 3 Hz when standing with eyes closed (Mauritz, Dichgans & Hufschmidt, 1979) whereas patients with Friedreich's ataxia affecting posterior columns and spinocerebellar input exhibit lower frequency (< 1 Hz) body movements which tend to have a stronger lateral sway component (Diener, Dichgans, Bacher & Gompf, 1984). Lesions of the vestibulocerebellar connections result in multidirectional low-frequency body oscillations (Diener et al. 1984) while patients with lesions of the cerebellar hemispheres have been found to be either indistinguishable from healthy subjects (Diener et al. 1984) or to show enhanced sway with a directional preponderance to the left and right (Umemura, Ishizaki, Matsuoka, Hoshino & Nozue, 1989). In some unilateral thalamic lesions (Masdeu & Gorelick, 1988) and unilateral basal ganglia lesions (Labadie, Awerbuch, Hamilton & Rapcsak, 1989) pronounced dysequilibrium can occur such that the patient often falls in a direction away from the side of the lesion. Patients with Wallenberg's syndrome following a lateral medullary infarct exhibit a diagonal pattern of body sway, from right forward to left backward for right sided lesions and from left forward to right backward for left sided lesions (Dieterich & Brandt, 1992). In an effort to understand such direction-specific postural deficits we have analysed some of the mechanical and neural factors that influence normal, residual body motion in three dimensions during quiet stance. When considering direction-specific instability it may be important to make allowance for mechanical differences in the skeletal structure between the sagittal and frontal planes. Structural differences in these two principal planes are

3 BODY MOVEMENTS WHEN STANDING 481 emphasized when a person stands with feet apart and it is a common experience that standing is sometimes made easier by adopting a wider stance. A healthy person may notice this fact only in situations that are particularly threatening to equilibrium such as when standing on a moving bus. Patients with problems of balance, however, often adopt a 'wide base' strategy quite naturally even in situations that are apparently undemanding. One obvious advantage of this strategy is that the area of support is increased as the feet are placed further apart and any disturbance of the position of the centre of mass would present less of a threat to lateral equilibrium. This is probably not the complete explanation since this strategy is not universally adopted by all patients with postural problems. The purpose of the present paper is to describe how in normal subjects different segments of the body move relative to each other in the two principal planes during quiet stance and how such movements are affected by altering stance width and removing visual information. Both of these factors are manipulated routinely in the clinical setting to test a patient's static postural ability by asking the subject to stand with feet together and eyes closed (Romberg's test). Visual input influences neural control of body sway. Stance width is thought primarily to be a mechanical factor, although we shall show with the aid of a mathematical model that it also exerts an important influence on the pattern of sway-induced afferent input. The way in which these two factors interact to influence the residual body movements during quiet stance provide some clues about the postural mechanisms used to achieve the task of bipedal stance. Part of these data have been published in brief form (Day, Steiger, Thompson & Marsden, 1990). METHODS With ethical committee approval thirty five normal male subjects were studied whose ages ranged from 29 to 63 years (45 9 ± 107 years mean + S.D.). Female subjects were not included in this study because of sex differences in the geometry of the skeletal frame and reported differences in the levels of baseline body sway (Overstall, Exton-Smith, Imms & Johnson, 1977). Subjects stood barefoot on a force platform (Kistler 9281B) facing and 1 m away from the corner of a room. The walls were draped with black curtains and a 1 cm red square was placed in the corner at eye height. When necessary, the wearing of spectacles was permitted to ensure that all subjects had normal binocular vision and were able to comfortably fixate this square. A non-contact, infrared motion detection system (Selspot II) was used to measure motion of various sites of the body in three dimensions. To achieve this, eight infrared-emitting diodes (IRED) were fixed with double-sided adhesive tape symmetrically on the left and right side of the back of the subject (Fig. 1) at the following levels: at the shoulders midway between acromion and mid-line; at the hips midway between anterior superior iliac spine and mid-line; at the knees in the popliteal fossa and at the ankles on the Achilles' tendon at the level of the malleoli. Stance width, or intermalleolar distance (IMD), was defined as the distance between the medial malleoli. Five IMDs (0, 4, 8, 16 and 32 cm) were studied in random order both with eyes open fixating the red square and with eyes closed. For each trial, subjects were asked to stand as still as possible with their hands together held relaxed in front of them while body motion and reaction force data were collected for 32 s. Data from the force plate and IREDs were digitized and collected with a sampling frequency of 100 Hz. Signal noise was reduced by averaging every four consecutive data points which lowered the effective sampling frequency to 25 Hz. This was considered an adequate sampling frequency since previous measurements of centre of pressure excursions that accompany body sway have shown that for young healthy subjects the principal power is contained in frequencies below 1 Hz whereas in some elderly subjects there may be additional low power components between 1 and 3 Hz (Lucy & Hayes, 1985). Even for posturally unstable

4 482 B. L. DAY AND OTHERS patients with cerebellar damage most of the power is contained in frequencies below 5 Hz (Mauritz et al. 1979). The raw data from the IREDs gave at each instant of time the three-dimensional position of each part of the body to which a marker was fixed. Digital differentiation of these signals gave the threedimensional velocity (speed and direction) of each body site. The following statistics were obtained Fig. 1. Experimental set-up showing the subject standing on the force plate with eight infrared-emitting diodes attached to his back at the sites shown, 0. Three cameras were used to view the diodes and to construct their three-dimensional position in space. Simultaneous recordings were made of the three components of force at each corner of the force plate from which the position of the resultant reaction force (centre of pressure) was calculated. directly from these data. Firstly, the mean speed of a body site which was given by the mean value of the magnitude of the velocity vector over the 32 s epoch. This measure is independent of the direction in which that part of the body moves. Secondly, the standard deviation of both the position and velocity traces at each site in the two principal directions of motion (anteroposterior (AP) motion in the sagittal plane and lateral (LAT) motion in the frontal plane) -over the 32 s epoch. These measurements quantify the change and rate of change of position of a body site about its mean values in the two specified directions. The standard deviation is numerically equivalent to the root-mean-square (RMS) of a signal that has a mean value of zero. For some analyses these

5 BODY MOVEMENTS WHEN STANDING 483 statistical values were averaged across all eight markers in order to obtain a single value that described the average behaviour of the whole body. This unweighted average makes no assumptions about the pattern of body sway that underlies the motion of each marker. For other analyses, values from markers on equivalent sites on the left and right side of the body were averaged to describe behaviour of the body at a particular level. % T L L w Fig. 2. Stick figure of skeletal structure in the frontal plane to explain the notation used in the mathematical model described in Methods and in the legends of Figs 8 and 9. It was also important to know about which of the main joints most of the body motion was occurring. This information could not be gained immediately from the measurements described above. For example, the markers at the shoulder level would move if the body rotated about either the ankle, the knee or the pelvis. On the other hand, simultaneous motion about two of those joints, if out of phase, may produce no motion at the shoulder. We were not able to measure true joint angular motion in three dimensions because that would have required either having markers located at the centre of rotation of the joint or else knowing its position relative to a given marker. Instead, our approach was to compute quasi-joint angle changes based on the relationship between the markers. This was done by joining consecutive markers with straight lines such that each side of the body was represented by a three segment linkage for which the angle between adjacent straight line segments could be computed. The three segments were at the top from shoulder to hip, in the middle from hip to knee and at the bottom from knee to ankle. The angle between the top and middle segment we shall term trunk angle and that between the middle and bottom segment we shall term knee angle. Since within a trial the feet did not move, the angle between the bottom

6 484 B. L. DAY AND OTHERS segment and the horizontal plane passing through the bottom marker was computed and termed ankle angle. As with the position and velocity information, we were interested to know how these angles changed over time and in which direction. Therefore, the angles were computed in twodimensions, as though the straight line segments were viewed from either the side (AP or sagittal plane) or the back (LAT or frontal plane) of the subject. The standard deviation of the resulting traces were computed to provide a measure of the changes in these quasi-joint angles over the 32 s epoch. The force plate gave data on the reaction force vector at each corner of the force plate. From this it was possible to measure both the resultant force vector and its point of application on the plate. The point of application was of particular interest as it was equivalent to the position of the centre of pressure of the feet. The standard deviations of the fluctuations in position and velocity of the centre of pressure in both the lateral and anteroposterior directions were computed over the 32 s epoch. Statistical analysis was performed using a 2 or 3 factor repeated measures analysis of variance. Biomechanical model of stance A mathematical model of the skeletal structure was developed to establish the theoretical relationships between lateral motion at different joints and of the head in the frontal plane and how these relationships are influenced by changes in stance width. In the frontal or lateral plane, if negligible movement of the knee joints occur then the joint angles of the hips and ankles must be related to each other by a function determined purely by the lengths of the four linkages. For a given stance width (W) therefore, a change in one joint angle leads to an inevitable and predictable change in the other three. Using the notation of Fig. 2 the angles of the right ankle, right hip and left hip are related to the left ankle in the following way: a= cos (P-Q) + Sin-' flr = sin() +sin-('lq), A=L 360 (al + an + fr Where, P= V(W2-2WLcos al+l2) Q I (W2-2WLcosaL+H2) 2 V(W2-2WL cosal+l2) R =LsincaL. If the head and trunk are assumed to be rigidly fixed to the pelvis then the tilt (y) and the lateral position (x) of the head also is a function of ankle angle and stance width, where: y - sin-' (sin ar-sinl))j X = + L (cos al-cos ar) -- (sin ao-sin al). 2 2 H RESULTS The motion of the body was deduced from the individual recordings of motion of each of the eight markers that were fixed to the back of the subject. The motion of each marker was resolved into motion in each of the three principal axes of the body. An example of raw data from one marker is shown in Fig. 3 and shows the velocity and position traces in these three directions together with the speed of marker.

7 BODY MOVEMENTS WHEN STANDING 485 Whole-body speed Subjects were instructed to stand as still as possible. The extent to which they were able to achieve this was reflected in the measurement of body speed, defined as the amplitude of the velocity vector irrespective of direction. Mean speed of the body was Lateral Anteroposterior Vertical Position Velocity L, Speed 8 s 10 mm 13 mms1 Pig. 3. Movement traces from the marker placed near the left hip of a 44-year-old man. For this 32 s trial the subject stood with his feet together (stance width = 0) and eyes closed. The position and velocity traces have been resolved into three components according to the principal axes of the body. The bottom trace illustrates the speed of the marker which is given by the amplitude of the vector sum of the three components of velocity. The thin horizontal lines on the velocity and speed traces denote zero levels. Note that motion is comparable in the lateral and anteroposterior directions and relatively small in the vertical direction. These and all other raw records in subsequent figures are taken from the same subject recorded during one experimental session. calculated by measuring the mean speed of each of the eight markers from the 32 s epoch and taking the arithmetic mean of those eight measurements for each stance condition. Figure 4 shows how the mean speed of the body was influenced by eye closure and stance width. Body speed was increased either by closing the eyes (F (1, 34) = 153-7, P < 0001) or by decreasing the stance width (F (4, 136) = 125-0, P < 0001). There was also a significant interaction between these two factors (F (4, 136) = 21X0, P < 0 001) indicating that removal of vision led to a greater increase in body speed the closer together were the feet. Whole-body velocity in sagittal and frontal planes Changes in the velocity of the body were analysed separately for the two principal planes of motion (lateral and anteroposterior). Since the subject stood without falling, the mean value of the component of velocity in any one plane was close to

8 486 B. L. DAY AND OTHERS A Eyes closed Eyes open O cm 4 cm mm 16 cm B 8 E -n 0) 4. o 0.0 b-0 C 0 16 Stance width (cm) Fig. 4. Influence of stance width and vision on mean speed of the body. A shows raw records of speed of the marker placed near the left shoulder of one subject when standing with eyes closed (left) or open (right) at three stance widths (0, 4, and 16 cm). Horizontal lines denote zero levels. B illustrates the group (n = 35) mean value (± s.em.) of speed over the 32 s epoch after averaging across the eight markers for each subject. Points shown are from subjects standing with eyes closed (@) or with eyes open (0). zero (Fig. 5A); movements in one direction were balanced by equivalent movements in the opposite direction. The standard deviation is a more important parameter as it describes the extent to which the velocity trace fluctuates about its zero mean 32

9 A Eyes closed Eyes open LAT velocity 0 cm I; ill klijs hi 1 L.IP AA.141 t Im 16cm L k IL, v I r-r 11 Al. I -WI w I 0 cm AP velocity 16cm I axki I jha,il PA!'M1J ALL. APw a B 6 Lateral sway 6 AP sway E E 3' 0-0> co E li L o--..o...o ' E Co 0 0~ E C 3. CD o Stance width (cm) 0* Stance width (cm) Fig. 5. Influence of stance width and vision on body motion in the frontal (LAT) and the sagittal (AP) planes. A shows raw velocity records from the marker placed near the left shoulder of a subject when standing with eyes closed (left) or open (right) at two stance widths (O and 16 cm). Horizontal lines denote zero levels. Note that the greatest change is seen in the lateral velocity trace when the subject stands with eyes closed and increases the stance width from 0 to 16 cm. B illustrates the group (n = 35) mean value (±S.E.M.) of the average standard deviation of the velocity fluctuations (top panels) and position fluctuations (bottom panels) in the frontal plane (left panels) and sagittal plane (right panels) over the 32 s epoch and across the eight markers for each subject Points shown are from subjects standing with eyes closed (O) or with eyes open (0).

10 488 B. L. DAY AND OTHERS A C of P - Velocity.. it;i,ii Ali j Position s-18a. s1 10 mm Shoulder - Hip - Knee - Ankle, r8 8 s... B 100 Position I VelocKtY n f'^ b%h10mm Velocity f M ) 30 mm s-1 2 s 0 1 Frequency (Hz) 2 C EU, cn :LI 0 E E c Ch 0o.0_ Stance width (cm) Stance width (cm) Fig. 6. For legend see facing page.

11 BODY MOVEMENTS WHEN STANDING value. The standard deviation about the mean was computed for each velocity trace in the two principal planes and this value averaged across all eight sites (Fig. 5B, top graphs). Qualitatively, the LAT and AP components of velocity behaved in a similar way. Both components were increased by eye closure (LAT: F (1, 34) = 115-6, P < 0-001; AP: F (1, 34) = 155-2, P < 0 001) and narrowing the stance width (LAT: F (4, 136) = 199-8, P < 0001; AP: F (4,136) = 38&7, P < 0-001). There was a significant interaction between the factors of vision and stance width (LAT: F (4, 136) = 44'2, P < 0 001; AP: F (4, 136) = 741, P < 0 001). Closing the eyes had a greater effect on velocity at narrower stance widths. There were two differences in the magnitude of these effects between the two components of velocity. First, increasing the stance width across the full range led to a much greater reduction in the lateral component of velocity compared to the AP component. Second, the interaction between vision and stance width also was numerically much greater for the lateral component. Thus, Romberg's quotient (value with eyes closed divided by value with eyes open) of lateral velocity changed from 1-50 with feet together to 1-03 at the greatest stance width. For the AP component the corresponding Romberg's quotients were 1-40 and 1'30. Whole-body position changes in sagittal and frontal planes Fluctuations in position of the body in the two principal planes were analysed in a similar way to the velocity changes (Fig. 5B, bottom graphs). In many respects the position data closely paralleled the velocity data. In both AP and lateral directions eye closure (LAT: F (1, 34) = 20-1, P < 0-001; AP: F (1, 34) = 48-1, P < 0 001) and narrowing the stance width (LAT: F (4, 136) = 107-6, P < 0 001; AP: F (4,136) = 3.3, P < 0 05) increased the fluctuations in body position with the effect of stance width being more potent in the lateral than in the AP direction. However, the strong interaction between stance width and vision that was present for velocity measurements was not significant for the position measurements (LAT: F (4, 136) = Fig. 6. Lateral motion in the frontal plane at different levels of the body and of the centre of pressure. A shows raw records of the velocity (left) and position (right) in the lateral direction from one subject of the centre of pressure (top) and of markers placed on the left side of the body at the levels near the shoulder, hip, knee and ankle when stood with feet together and eyes closed. Horizontal lines on the velocity traces denote zero level. Note that velocity of centre of pressure attains much higher values than any site on the body. The traces from the shoulder marker and the centre of pressure over the time interval defined by the dotted boxes of A have been expanded and superimposed at the top of B (position traces were superimposed by eye). The trace from the shoulder marker is the darker of the two. Note that the major difference between the velocity fluctuations of the centre of pressure and that of the body occurs in the higher frequency band. The bottom graph of B shows superimposed the velocity frequency spectra of the centre of pressure and of the shoulder computed from the full 32 s recorded length. The differences between these two spectra have been emphasized by shading between them at those frequencies when the amplitude of the centre of pressure spectrum was greater than that of the shoulder. The two spectra deviate appreciably only at frequencies above 05 Hz. C illustrates the influence of stance width on lateral velocity (left) and position (right) fluctuations in the frontal place. The open symbols represent the group (n = 35) mean values (+ S.E.M.) of the standard deviation of lateral motion over the 32 s epoch averaged across the two markers placed on the right and left sides at the level of the shoulders (KO), hips (0), knees (V) and ankles (A\). M, Group mean value (±s.e.m.) of standard deviation of lateral motion of the centre of pressure. 489

12 490 B. L. DAY AND OTHERS A LAT AP Trunk Knee Ankle B 0o4. C) a) -0 Qc CD 02- Lateral sway <\Eyes open X. usg _0 - '* h-&. - < 1 deg 8 s co a)0 -a 0.4- AP sway Eyes open O i ) -a a) C c Eyes closed - 4.ran _0 %4^ 0) X1 CD M7 02 in Eyes closed _F O Stance width (cm) 32 oj Stance width (cm) Fig. 7. Influence of stance width on angular fluctuations between adjacent body segments in the frontal plane (LAT, left panels) and sagittal plane (AP, right panels). A shows raw traces of computed angles from the right side of one subject standing with feet together and eyes open. Note the lower frequency dominance of the 'trunk' movements in the AP direction compared to those of the ankle in the LAT direction. B shows group (n = 35) mean (+ S.E.M.) values of standard deviation of angular fluctuations over the 32 s epoch for the trunk angle (5), the knee angle (A) and the ankle angle (0). See Methods for definition of 'angles'. Data were obtained from subjects standing with eyes open (top panels) and eyes closed (bottom panels).

13 BODY MOVEMENTS WHEN STANDING 2X0, P > 0 05; AP; F (4, 136) = 05, P > 005). Closing the eyes, therefore, increased the fluctuations in body position by an amount that was independent of stance width. Motion of centre of pressure and of body at different levels These data were plotted separately for each level of the body (two IREDs per level). There was an orderly increase in amplitude of both the velocity and position fluctuations from markers placed progressively higher up the body. This is illustrated in Fig. 6 for movements recorded in the frontal plane with eyes closed. Similar relationships were obtained for movements with eyes open and for movements in the sagittal plane. The equivalent motion of the centre of pressure as it moved over the surface of the force plate is shown in the graphs of Fig. 6. The fluctuations in position of the centre of pressure were similar to those recorded from the body at the level of the hip markers. The shoulder markers moved more than the centre of pressure while those at the knees and ankles moved less. In contrast, the amplitude of the fluctuations in the velocity trace was always considerably greater for the motion of the centre of pressure than for any site on the body. Angular motion between body segments The angular fluctuations between one body segment and its neighbour were estimated from the standard deviation of the angle formed between adjacent straight lines joining the markers (see Methods). These data are shown for eyes open and closed for the two principal planes in Fig. 7. Three stance widths (0, 8 and 32 cm) were considered in the statistical analysis. In both planes the angular fluctuations were significantly influenced by stance width (LAT: F (2, 68) = 68-0, P < 0 001; AP: F (2, 68) = 15-4, P < 0-001), vision (LAT: F (1, 34) = 8-0, P < 0-01; AP: F (1, 34) = 14.4, P < 0-01) and the 'joint' examined (LAT: F (2, 68) = 38-3, P < 0-001; AP: F (2, 68) = 25-5, P < 0-001). The only difference between angular fluctuations in the two planes was the significant interaction between stance width and 'joint' in the frontal LAT plane which was not present in the sagittal AP plane (LAT: F (4,136) = 53 9, P < 0 001; AP: F (4, 136) = 1'4, P > 0 05). This significant interaction term in the frontal plane was due to the disproportionate reduction in angular fluctuations about the ankle as the stance width was increased. All other interaction terms were not significant. In the sagittal AP plane, therefore, most angular movement occurred between the trunk and upper leg for all stance widths. In the frontal LAT plane, most angular movement occurred between the trunk and upper leg for stance widths above 8 cm but angular motion about the ankle dominated when the feet were closer together. 491 DISCUSSION Direct measurement of body movement confirmed that vision and stance width influence the amplitude and velocity of body sway during quiet stance. Similar effects on the amplitude of body sway have been reported in previous studies that relied on measurement of motion of the head (Miles, 1922), of the centre of foot

14 492 B. L. DAY AND OTHERS pressure obtained from ground reaction forces (Okubo, Watanabe, Takeya & Baron, 1979; Paulus, Straube & Brandt, 1984; Kirby, Price & Macleod, 1987) or from accelerometers placed at different levels of the body (Amblard, Cremieux, Marchand & Carblanc, 1985). The present data extend these observations by describing: (1) how body motion relates to centre of pressure motion; (2) how the motion is distributed across the body in three dimensions and (3) the way in which the two factors of vision and stance width interact. Relationship between body motion and centre of pressure motion The movement of the centre of pressure was not identical to movement of the centre of mass of the body. Although the amplitude of travel of the centre of pressure as it moved over the surface of the force plate was similar to that of the hip markers, it attained higher velocities than any level of the body. This dissociation between body motion and centre of pressure motion has been suggested previously on theoretical grounds (Thomas & Whitney, 1959; Gurfinkel, 1973) and arises from dynamical effects which are frequency dependent. If the body were inanimate and motionless then the centre of pressure would necessarily lie vertically beneath the centre of mass. For the human subject trying to stand as still as possible this is an active process. Motion of the centre of pressure is achieved partly by passive elastic restoring forces, which develop as tissues are stretched by body movement and partly by changes in muscle activity. The net muscular forces shift the position of the centre of pressure and accelerate the body in the opposite direction. For example, a body falling forwards can be arrested by a plantarflexing torque about the ankle which moves the centre of pressure forwards and accelerates the body backwards. The rate of movement of the centre of pressure, if negligible deformation of the feet is assumed, depends exclusively upon the rate of build-up of force by the muscles. The acceleration of the body will depend also upon the mass of body which is sufficiently large to ensure that the rapid and presumed small adjustments of muscle activity that occur during quiet stance produce faster changes of position of the centre of pressure than of the body. The inverted pendulum model of body sway The inverted pendulum model of body sway has been used extensively to describe AP body motion either during quiet stance or when external disturbances are applied and assumes that movement occurs exclusively about the ankle joint (Smith, 1957; Gurfinkel & Osevets, 1972; Gurfinkel, Lipshits & Popov, 1974; Nashner, 1976; Fitzpatrick, Taylor & McCloskey, 1992). Others have questioned this model (Thomas & Whitney, 1959; Roberts & Stenhouse, 1976; Woollacott, von Hosten & Rosblad, 1988). The present data show that movement is distributed across the body in such a way that those body segments further from the ground move faster and further than those closer to the ground. In this respect the body moves in a way predicted by the inverted pendulum model. However, the same data analysed according to amplitude of angular rotation between adjacent body segments suggest that this model is incomplete. In the sagittal AP plane most angular displacement occurs between the trunk and the leg under all conditions studied although it should be pointed out that the 'trunk' angle consists of a combination of pelvis and vertebral

15 BODY MOVEMENTS WHEN STANDING 493 movements. The situation is similar for lateral movement in the frontal plane with stance widths greater than 8 cm; only with narrower stance widths does motion about the ankle joint dominate. The inverted pendulum model, therefore, seems applicable only under restricted conditions although it is worth noting that a given rotation about the ankle joint would produce greater displacement of the top of the body compared to that produced by the same angular rotation about the hips. It seems that the body is potentially unstable at many levels, not just at the ankle joint, and that at each joint movement needs to be detected and actively corrected in order to minimize the net body motion. A mechanism of lateral stabilization Movement was reduced in both the frontal (i.e. lateral motion) and to a lesser extent in the sagittal (i.e. anteroposterior motion) planes by increasing stance width. The greater effect in the frontal plane was due largely to the reduction in lateral rotation about the ankle joints and feet. This phenomenon can be explained by an important mechanical difference in the body structure between these two planes. In the sagittal plane AP motion is possible at the ankle, knee and hip joints independently. This is not possible for lateral movement in the frontal plane, the hips and ankles are linked together so that a change in one joint angle leads to a predictable change in the other three provided there is negligible movement of the knee joint. In normal circumstances lateral movement of the knee is very restricted and AP movement of the knee is limited when it is locked in hyperextension. Indeed, the present data show that little angular motion occurred at the knee joint, especially in the lateral plane. The mathematical relationships between the ankle and hip joint angles are described in Methods and an example using a specific body geometry is shown graphically in Fig. 8. The most important point of these relationships is that the strength of the mechanical coupling between the ankles and the hips is dependent upon stance width. If it were possible to stand with both ankle joints coincident there would be zero mechanical coupling between the ankles and hips. The only muscles able to prevent lateral rotation of the ankles would be those that evert or invert the ankles. As the feet are moved apart a change in ankle angle is accompanied by a change in hip angle, the amount of which increases with stance width. Thus, the strength of the coupling between the ankles and hips increases with stance width such that lateral movement about the ankles can be increasingly controlled by muscles that abduct and adduct the hips and vice versa. In other words, the structure can be made effectively stiffer simply by increasing the stance width and keeping the stiffness of each of the four joints constant. The increase in passive stiffness of the structure is not the only consequence of the coupling between ankles and hips. The variable strength of coupling also influences the pattern of afferent input produced by a given ankle movement. As the strength of the coupling increases with stance width, any ankle movement leads to greater movement of the hips and greater stretch of hip muscles. Proprioceptors located in the muscles and joints of the hips will increasingly participate with those of the ankles in signalling lateral motion of the structure about the ankles. This increase in proprioceptive sensitivity to lateral motion would assist central postural mechanisms

16 494 B. L. DAY AND OTHERS A B Left hip ~~~~~~~~~~Right hip 0 Change of hip angle (As) \/ ~~~~~~~~~2 deg 4 deg Change of left 2dg 4 ankle angle \40 cm (AaL) Stance width (W) c ~~~~~~~~~~~D Right anklde >9 Change (AXtj(AaR) of olefth age ankle angle le 40cm ankle angle ccm f \ (ACXL)/ \ / Stance width (W) Fig. 8. Theoretical relationship between angles of ankle joints (a) and hip joints (/1) in the frontal plane as a function of stance width (W). D illustrates how the left hip joint angle changes with the ankle joints when the feet are apart but not when the feet are together, provided movement at the knee is ignored. The three surface plots describe the relationships for a specific body geometry between imposed changes of the left ankle and the resulting changes of the left hip (A), right hip (B) and right ankle (C). For each plot a horizontal surface is drawn which denotes zero change in the 'joint' angle under study. The origin of each of these three dimensional graphs is shown by the three axes system labelled 0. The increase in the strength of coupling between the ankle and hip joints is reflected in the increasing slope of the curve as the stance width is increased (A and B). The values plotted were derived from the mathematical model described in Methods. For each stance width (O to 40 cm in 4 cm increments) the left ankle angle was changed + 5 deg (in 0 5 deg increments) about that angle obtained with the body positioned symmetrically around the midline. Plotted are the resulting changes in joint angles relative to their respective angles of symmetry. The parameters of the model were set as follows: distance

17 BODY MOVEMENTS WHEN STANDING since they rely on accurate and sensitive detection of movement before they can issue appropriate compensatory motor commands. It is likely, therefore, that part of the observed reduction in lateral body motion with stance width is due to central machinery taking advantage of the increased proprioceptive sensitivity to that motion. Paulus et al. (1984) showed that visual stabilization of body sway depends critically upon the characteristics of the visual scene. For example, they found that lateral body sway and eye-object distance were linearly related such that sway decreased with decreasing eye-object distance. They explained this result as being due to improved resolution in the detection of head motion through the geometric consequence of greater retinal shifts of the visual image with a decrease in eye-object distance. The decreasing effectiveness in the ability of vision to reduce lateral sway with increasing stance width observed in the present experiments may occur for similar reasons. The sensitivity of visual and vestibular detection of lateral body sway may be influenced by the mechanical coupling between the ankles and the hips. The reason for this is that movement of the pelvis determines, to some extent, movement of the head and movement of the pelvis, in response to rotation of the ankles, is critically dependent upon stance width. In fact, movement of the head produced by rotation at the ankles depends not only upon the geometry of the legs and pelvis but also on how neck and vertebral joints move at the same time. For simplicity we shall assume that such additional motion is negligible, as if the head were rigidly connected to the pelvis by a stiff bar, so that movement of the head in response to ankle rotation is solely a function of stance width (again assuming negligible knee movement). We can describe head movements in terms of tilt with respect to gravity plus lateral translation. These mathematical relationships are described in Methods and an example is shown graphically in Fig. 9. As the feet are moved apart the lateral tilt of the head produced by a disturbance to the ankle becomes smaller until a position is reached (when the distance between ankles equals the distance between hips) at which no tilt occurs (although translation of the head would still occur). At still greater stance widths the head tilts in the opposite direction to that when the feet are together. A similar picture is obtained if lateral translation of the head is considered, although greater stance widths are required before the point is reached at which zero translation occurs and above which the head moves in the opposite direction. The simple act of increasing the stance width, therefore, may diminish or even reverse the direction of the response of headmounted receptors to a rotation about the ankle. It is not yet clear how the postural centres make use of such stance dependent patterns of afferent information. One approach to this question would be to measure the induced postural response to a change in afferent input under different stance conditions. Preliminary results from experiments in which lateral postural responses were produced by a change in vestibular input show that the postural response is attenuated by increasing stance width (Day, Pastor & Marsden, 1992). These findings suggest that the central gain from ankle to hip (L) = 95 cm and distance between hips (H) = 25 cm. These values were taken from approximate measurements on one of the authors. The relationships shown in the figure were qualitatively similar over a wide range of parameter values. 495

18 496 B. L. DAY AND OTHERS A Lateral translation Lateral translation of head (AX) 6 cm Change of left deg 40 cm ankle angle Stance (Aad) width (W) Bi C Change of left ankle angle (SAcL) \t ~~~~TilIt ofa head 4 (y)) 2 deg 2c 2 deg i m Stance width (W) Fig. 9. Theoretical relationship between head motion/orientation and changes in ankle joint angle in the frontal plane. C illustrates how lateral translation and tilt of the head changes in one direction with the ankle joints when the feet are together but in the opposite direction when the feet are apart, provided movements at the knee, vertebral column and head are ignored. The two surface plots describe the relationships for a specific body geometry between imposed changes of the left ankle and the resulting lateral head displacement (A) and lateral head tilt (B). For each plot a horizontal surface is drawn which denotes zero displacement or tilt. The origin of both of these three-dimensional graphs is shown by the three-axes system labelled 0. The change in the relationship between the ankle and head movements is reflected in the changing slope of the curve as the stance width is increased. The values plotted were derived from the mathematical model described in Methods. For each stance width (O to 40 cm in 4 cm increments) the left ankle angle was changed + 5 deg (in 0 5 deg increments) about that angle obtained with the body positioned symmetrically around the midline. Plotted are the resulting changes in lateral position (X) and tilt (y) of the head. The parameters of the model were set as follows: distance from ankle to hip (L) = 95 cm; distance between hips (H) = 25 cm and distance from pelvis to eyes (T) = 70 cm. These values were taken from approximate measurements on one of the authors. The relationships shown in the figure were qualitatively similar over a wide range of parameter values.

19 BODY MOVEMENTS WHEN STANDING of vestibular control of lateral sway may be changed according to the stance conditions. In the present experiments it is interesting that vision was found to be less effective in reducing lateral body velocity with larger stance widths. This may be because vision becomes less effective in detecting lateral motion, as outlined above, or it may merely reflect a 'ceiling' effect due to the limitations of either the visual detection system or the motor system as the baseline body motion diminishes with stance width. Cross-talk between the sagittal and frontal planes The effects of vision and stance width on AP motion in the sagittal plane in some respects were similar to those observed in the frontal plane. AP body motion was reduced by opening the eyes or by increasing the stance width and there was an interaction between these two factors on body velocity. The effect of vision in helping to minimize AP body motion is explained by changes in visual signals or changes in eye position contributing information on body motion in that plane. The effects of stance width are more difficult to explain since there is no obvious change of the body structure in the sagittal plane with stance width. We favour the view that lateral and AP body motion are not completely independent so that motion in one plane can somehow be reflected in the other plane, but in an attenuated form. One possible explanation is that a number of muscles control movement in both planes and provide a means by which movement can overflow from one plane to the other. For instance, a slightly incorrect pattern of muscle activation around a joint may successfully correct a disturbance of the body in the frontal plane but initiate a disturbance in the sagittal plane. The size of this overflow (or error) may be related to the magnitude of the original disturbance. Against this is the finding that the reduction in AP angular motion between adjacent body segments with stance width was the same for all three 'joint' angles unlike the situation in the lateral direction. An alternative explanation is that the apparent cross-talk reflects a property of the central controlling mechanisms. For example, it may be that postural centres are able to control AP motion more efficiently once the overall body motion has been reduced. This could take place through a heightening of sensory detection or an improvement in accuracy of motor output or even through a shifting of computational resources away from control in the frontal plane to the sagittal plane. The present study has described the behaviour of the body when standing and some of the mechanisms that may contribute to this behaviour. From a theoretical viewpoint, one of the interesting ideas to emerge is that the absolute and relative sensitivity of different modes of afferent input in response to disturbances of the body is highly dependent upon the initial posture. With increasing stance width lateral body motion is detected more easily by proprioceptors and less readily by eyes or vestibular organs. From a practical point of view, this theoretical framework may help us to understand the various patterns of excessive body movements seen in patients with different lesions of the nervous system and help to disentangle some of the mechanical and neural factors which contribute to the underlying balance problem. 497

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