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1 Department of Physical Therapy and Human Movement Sciences, The Feinberg School of Medicine, Northwestern University, Chicago, IL;; 2 Prince of Wales Medical Research Institute and University of New South Wales, Sydney, NSW 2031, Australia
Submitted 29 October 2002; accepted in final form 2 April 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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), are used when disturbances are small. The ankle strategy is
dominant for the smallest disturbances, whereas the hip strategy is more
important when disturbances are larger or when the BoS is limited
(Horak and Nashner 1986;
Nashner and McCollum 1985;
Shumway-Cook and Woollacott
2001). Protective strategies, the most common of which is
stepping, are considered to be last-resort responses that are initiated when
the center of mass (CoM) of the body passes outside the limits of the BoS so
that balance cannot be maintained without reconfiguring the BoS by active
movements such as stepping (Shumway-Cook
and Woollacott 2001).
This hierarchical model of strategy selection according to the amplitude of
the postural challenge is at odds with observations that subjects step more
often than expected by this criterion when they are instructed to react
naturally (Brown et al. 1999;
Maki and McIlroy 1997;
Rogers et al. 1996) and that
stepping is often initiated very rapidly well before the limits of the BoS are
reached (Pai et al. 2000).
Thus stepping does not depend solely on the mechanical constraints of the
position of the CoM exceeding the BoS. A more complex mechanical model that
includes the velocity of the CoM and momentum of the body rather than just the
position of the CoM is an improvement (Pai
and Patton 1997) and more reliably predicts stepping during
waist-pull and support-surface perturbations (Pai et al.
1998,
2000). However, subjects still
step more often than predicted by this model and, on average, older
individuals step more often and with smaller perturbations than younger adults
(McIlroy and Maki 1993;
Pai et al. 1998;
Rogers et al. 2001b). This
suggests that physiological factors, at this stage unknown, rather than
mechanical factors are likely to determine step initiation.
Age-related changes in the sensorimotor and neuromuscular physiology
critical for postural control are the likely candidates to explain the
different stepping behavior in older people. Visual changes include reduced
acuity, contrast sensitivity, and depth perception
(Pitts 1982). Somatosensory
changes include reduced proprioceptive, touch-pressure, and vibration
sensibility, particularly in the lower limbs
(Kenshalo 1986;
Skinner et al. 1984).
Neuromuscular changes with aging include reduced muscle strength and mass
(Merletti et al. 2002;
Vandervoort 2002) and delayed
reaction times (Welford 1988).
All of these factors are associated with balance disorders and an increased
risk of falls (Lord et al.
1991).
The present study investigates the displacement–velocity threshold
for triggering protective stepping during waist-pull perturbations of stance.
When a postural perturbation occurs, the CoM–BoS relationship is
disrupted and the subject must perform compensatory strategies to maintain
postural balance. Regardless of the exact site where the perturbation may be
applied, the common key relationship among various perturbation methods is the
change in orientation of the CoM relative to the BoS. It is likely that
differences between subjects in their abilities to compensate for disturbances
of balance reside in their control of protective stepping responses, and other
strategies, rather than in the means of perturbation that precipitates the
condition of falling. Waist-pull perturbations were used to alter this
relationship because of the precise control over the mechanical perturbation
parameters that the device provided
(Pidcoe and Rogers 1998).
Young and older adults are studied to identify physiological factors
associated with step initiation.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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Twenty-four young subjects, 18 women and 6 men, aged 21–37 yr (mean age: 25.3 ± 4.2; weight: 68.1 ± 14.9 kg; height: 1.68 ± 0.09 m) were recruited from the staff and students of the university. Twenty-five older subjects, 15 women and 10 men, aged 60–85 yr (age 71.8 ± 7.0; weight: 71.1 ± 13.2 kg; height: 1.64 ± 0.11 m) were recruited from among community-dwelling elderly people. Subjects underwent a standardized telephone screening administered by a physical therapist and were included only if they had no significant neurological (stroke, Parkinson's disease, peripheral neuropathy), musculoskeletal (joint replacement, leg or back pain, or any other limitations), or other medical disorders (depression, cardiac, metabolic, or respiratory problems) that affected functional movement performance. Older subjects were included only if they had no previous history of falls. The Institutional Review Board of the Northwestern University in accordance with the 1964 Helsinki Declaration approved the study, and subjects provided written informed consent.
Protocol
STEPPING RESPONSES. Subjects stood on two separate force
platforms (AMTI, Newton, MA) that recorded forces under each foot. They took a
natural and comfortable foot position that was then maintained for each trial.
Stepping was induced by a constant-velocity forward pull from a linear motor,
delivered by a flexible cable that was attached to a belt that subjects wore
at the level of the pelvis (Fig.
1A, Pidcoe and Rogers
1998). The pulls started at an unexpected time and proceeded at
the test velocity until, on reaching the test displacement, the cable tension
was released. If a step had not already been initiated, the subject could lean
back to his or her initial position (Fig.
1A, profile). Subjects' use of limb and other segmental
movements was not constrained. They wore a safety harness that did not
restrict movement.
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The test protocol was 124 waist pulls with different velocity–displacement combinations (Fig. 1B). These were derived by pairing 8 displacements (4–18 cm in 2-cm steps) and 23 velocities (2.25 to 305 cm.s–1 on an exponential scale: v =1.8 x 1.251,2...23). Before they were administered, subjects had 8 practice trials, one at the mid-velocity of each displacement (Fig. 1B, shaded). Subjects were instructed to "try not to step" in response to the pulls. To minimize fatigue, the 124 combinations were presented as 2 sets of 62 with 10 min of rest between them (triangles and circles, Fig. 1B). In the second set, the combinations that were most difficult to resist (open circles) were not delivered if all the perturbations around them had induced a step in the first set of perturbations. Within each set, the velocity and displacement combinations were randomized.
The force plate and motor position data were sampled at 100 Hz by an A-D converter and stored on computer. The onset of the pull started 1 s after the onset of the record.
SENSORIMOTOR FUNCTION. Six tests of sensorimotor function
considered to be important for postural control and having good
test–retest reliability (Lord et al.
1991; Lord and Castell
1994) were administered over 1 h. The tests were 1)
vibration sense, 2) touch-pressure sensation, 3)
proprioception, 4) visual acuity, 5) ankle plantar-flexion
strength, and 6) foot voluntary reaction time.
Vibration sense at the tibial tuberosity was measured with an amplitude-controlled vibrator at 200 Hz. The vibrator had a 10-mm hard rubber dome that rested on the skin with a constant 1 N background force. In each trial, the vibration amplitude (0–100 µm) was either slowly increased from an imperceptible level until the subject reported the vibration or slowly decreased from a clearly perceptible level until the subject reported that the vibration had ceased. Threshold for perception of vibration was calculated as the mean intensity of six alternate trials on the dominant leg.
Touch-pressure sensation at the lateral malleolus was measured with a Semmes–Weinstein aesthesiometer. This consists of a set of 20 calibrated nylon monofilaments that applied forces between 4.5 mg and 447 g. Thresholds were obtained by a forced-choice paradigm, the subject nominating on which of two occasions the ankle was touched. After three trials, a smaller stimulus was applied if all three responses were correct, or a larger stimulus was applied if one was not correct. Using this stepwise threshold tracking procedure, the threshold was taken as the smallest of the last three stepwise reversals.
Proprioception was assessed with lower-limb matching task in which subjects were seated and with the eyes closed actively lifted each leg and aligned the big toe of each foot on opposite sides of a large (60 x 60 cm) clear protractor placed vertically between the legs (De Dominico and McCloskey 1987). Performance was recorded as the mean error in degrees of five matching trials.
Visual acuity was measured using a high-contrast Snellen chart read at 4 m in a standardized well-lighted room. Acuity was recorded as the minimum angle resolvable on a logarithmic scale (logMAR).
Ankle plantar-flexion strength was measured in the dominant leg during maximal isometric and isokinetic contraction with a Biodex System 3 Pro (Biodex Medical Systems, Shirley, NY) sampled at 100 Hz. The dominant leg was that which the subject would use to kick a ball. Subjects sat in a chair with the trunk inclined at 70°, the thigh approximately horizontal, the knee positioned at 30° of flexion and the ankle at 90°. The foot was firmly strapped to a plate. Isometric plantar-flexion strength was measured by instructing subjects to "push the plate as fast and hard as you can" for 5 s. They performed 3 trials of 5-s duration with 10 s of rest between each trial. The best of the 3 trials was chosen as the plantar flexion peak torque, and the torque rate was calculated as the peak torque divided by the time to peak. Isokinetic plantar-flexion strength was tested at 60 deg.s–1. Subjects were instructed to "push and pull the plate as hard and fast as you can." Plantar-flexion strength was chosen as the mean of the three highest peak torques for the five repetitions. Because strength is critically linked with the load it has to move, the ankle strength values were normalized to the weight x height product of each subject for statistical analysis. The assumption is that the required torque to move the body about the ankles is proportional to the mass and the height of the CoM.
Simple reaction time was measured as the mean of 10 trials in which subjects used the dominant foot to react to a bright red 10-mm LED. A variable delay period separated repeated presentation of the stimulus cue.
Data analysis
With small amplitude perturbations, the body tends to behave like a
simple-inverted pendulum, whereas with larger amplitude it behaves more like a
double-inverted pendulum (Nashner and
McCollum 1985). Nevertheless, the final position of the pelvis at
the end of the perturbation reflects the initial position of the body and the
size of the perturbation. This initial position relative to the ankles
(Fig. 1A, CoPi) can be
estimated from the mean CoP position during the second before the pull.
Because previous experiments have shown a comparable motion profile between
the pelvis and the motor for this device
(Pidcoe and Rogers 1998), the
final position of the pelvis at the end of the perturbation was calculated for
each trial by adding the displacement of the pull (D) to the initial position
of the CoP (CoPi). This position (Fig.
1A, P) was calculated in reference to the ankle position
and thus it reflects how far forward the pelvis is from the ankles at the end
of the pull. This position, the velocity of the pull, and the response to step
or not, characterized each trial. From these data, a total stepping record for
the array of perturbations was compiled for each subject.
INDIVIDUAL THRESHOLD BOUNDARIES. For each velocity for which it was possible, a position threshold was determined as the midpoint between the largest value of position (P) (i.e., the most forward position) without a step and the smallest value of P (i.e., the closest position from the ankle) with a step. After inspection of these data, a sigmoidal relationship between position and velocity was apparent. A Boltzmann sigmoidal function was fitted to these position points (Gauss–Newton, nonlinear, least-mean-squares) to describe a position threshold for stepping as a function of velocity (Fig. 2B, equation and graph). The four parameters estimated were the threshold plateaus at low (TL) and high (TH) velocities, the velocity (V50) that produces the midrange response, and the slope (S) of the relation at midrange.
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GROUP STEPPING BOUNDARIES. Ideally, a threshold, or midpoint, could be calculated for each of the 23 velocities for each subject. However, some subjects never stepped or stepped for all pulls at extreme velocities so the midpoint was undefined. Therefore the individual threshold boundary for a subject was not calculated if <12 of the 23 threshold points were defined. This excluded five young subjects from the individual analysis. In addition, the threshold boundary for a subject was also not included in the individual analysis if the range of perturbations was insufficient to capture the sigmoidal shape. The criterion for this was if r2 <0.70 for the Boltzmann function fit. This excluded seven older subjects from the individual analysis. To include these missed subjects in the analysis, a position boundary for producing 50% stepping for the group was calculated from the stepping frequencies for all subjects to all perturbations. For each velocity, the position at which the subjects stepped in 50% of the trials was estimated, and these points were then fitted with the Boltzmann sigmoidal function to produce the group position boundary.
STATISTICAL ANALYSIS. To assess aging changes in stepping thresholds, each parameter of the equation was submitted to an analysis of variance with group as the between factor. Pearson correlation coefficients were calculated to assess the associations between the anthropometric, sensorimotor, and neuromuscular variables and the stepping parameters TL, TH, and V50. Partial correlations were then calculated to assess these associations while controlling for age group.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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Individual threshold boundaries
Responses obtained during a full set of trials are shown in Fig. 2A for typical younger and older subjects. The demarcation between the position that causes subjects to step (shaded circles) or not (open circles) is obvious. Thus the position threshold points (diamonds), midway between the most anterior position without a step and the closest position from the ankle with a step, form a narrow band across the domain of pull velocities. Inspection of these data points indicates asymptotes at low and high velocities where the threshold is independent of velocity. Between these asymptotes, threshold is inversely related to the velocity.
To select a model to describe this threshold response, it is necessary to consider the physical effects of an external perturbation on stance. The fundamental requirement for standing equilibrium means that if the perturbation is large enough to move the CoM beyond the limits of the BoS, a step must be taken. This upper limit of the perturbation for stepping applies for all velocities, no matter how slow. As velocity increases, momentum becomes more significant. Thus the threshold position should move progressively closer to the ankle so that the momentum of the body produced by the forward pull can be overcome before the CoM reaches the anterior limit of the BoS. In actual subjects, another factor places a lower limit on the perturbations that will produce sufficient body movement to cause stepping. The energy of an external perturbation that is transferred to the body can take two forms: kinetic energy associated with the movement of the body; and potential energy, which may be elastic and held by deformation of the tissues and body segments, or gravitational through any elevation of the CoM of the body. Here, the gravitational energy should be trivial because the motor pulls horizontally at approximately the height of the CoM. However, as the amplitude of the displacement becomes smaller at high velocities, a greater proportion of the energy will be taken as elastic energy by the soft tissues and joints because of their lower short-range stiffness. Eventually, when all of the perturbation is ineffectively taken as potential energy, forward body movement will be insignificant so that there is no need to step. Thus this is a system with a region of transition between two limiting states that are independent of the input variable, velocity. Stepping will always occur when the perturbation pulls the CoM in front of the BoS, and stepping will never occur when the perturbation is below a critical level that does not require a response.
Both the theoretical considerations and the empirical observations
illustrated in Fig. 2 indicate
that a Boltzmann function of velocity would be ideal to model the threshold
boundary for stepping. This sigmoidal function describes systems that have a
transition between distinct response limits for high and low input values
(Capaday 1997). It takes the
form shown in Fig. 2B,
and is described by four parameters: the high-velocity threshold
(TH), the low-velocity threshold (TL), the velocity
(V50) that produces the midrange response, and the slope (S) of the
relation. The inverse of the slope is directly proportional to the maximal
steepness of the function, which occurs at V50. Of the 49 subjects,
42 had an r2 >0.70 for the Boltzmann function fit, and
the remaining seven failed to reach this criterion through insufficient data
rather than an apparent different pattern of the threshold boundary.
Group threshold boundaries
The position and velocity data of each subject were expressed as %BoS and %BoS.s–1, respectively, and pooled to find a threshold boundary that would cause stepping in 50% of all trials for each group. The relative frequency of stepping for the group (0–1) is plotted against the position (%BoS) and velocity (%BoS.s–1) for the young and old groups in Fig. 3. At all velocities, the group never stepped (frequency = 0) when the position of the pelvis was close to the ankles, whereas they stepped in most of the trials (frequency = 1) when the pulls moved the pelvis beyond the limit of the BoS. On the slope between the base level (dark shading) and the plateau (white), stepping frequency increased as the final position increased anteriorly. At each velocity, the point halfway up the slope (frequency = 0.50) can be identified by fitting a Boltzmann function to the stepping frequency data with position as the independent variable. This function with its 0.50 point is illustrated for one velocity as "F = f (vi, P)" in the top of Fig. 3. For all velocities tested, these points form across the contour of the sloped surface a curve that describes the position that produces stepping in half of the trials. Like the individual threshold boundaries, this position that produces 50% stepping for the group is also best described by a Boltzmann function of velocity (Fig. 3, "C"). These group functions, which we refer to as "position boundaries for 50% stepping," are analogous to the individual threshold boundaries described above. The fit of Boltzmann functions to these group data were very accurate; r2 = 0.995 for the young group and r2 = 0.993 for the older group. In these plots, there are clearly well-defined low-velocity (S50L) and high-velocity (S50H) plateaus, providing further support for the choice of the Boltzmann model to describe the stepping behaviors of individual subjects.
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Age, stepping frequency, and thresholds
The S50L (74% versus 108% BoS) and the S50H (52% versus 72% BoS) of the group boundaries for 50% stepping were both lower for the old than for the young. Likewise, the V50 of the group boundaries was a lower velocity (109% vs. 129% BoS.s–1) for the old than for the young. The slope tended to be smoother for the old (0.316) than for the young (0.180). From the shape of the stepping records of the young and older groups in Fig. 3, it is clear that the total number of steps taken, which is related to the volume of the hill, will be associated with the parameters of the position boundaries for 50% stepping. The overall stepping frequency for all subjects was 32% (±15) of pulls for the younger group and 56% (±11) for the older group.
Averaging the parameters of the individual threshold boundaries (Fig. 4) gave results consistent with the group position boundaries for 50% stepping. TL was lower (closer to the ankle) in the older subjects than in the young [17.0 ± 2.5 vs. 20.7 ± 1.9 cm, F(1,35) = 24.7; P < 0.001]. The BoS was also shorter for the older subjects than that for the young [18.5 ± 1.6 vs. 19.9 ± 2.4 cm; F(1,47) = 6.2; P < 0.02]; however, TL was still smaller for the old [91 ± 12 vs. 107 ± 10% BoS; F(1,35) = 19.7; P < 0.0001; Fig. 4, left] after normalizing to the length of BoS. Similarly, TH was lower for the old than for the young, both in absolute terms [11.1 ± 1.8 vs. 13.9 ± 1.8 cm; F(1,35) = 23; P < 0.001] and when normalized to the BoS length [59 ± 8 vs. 72 ± 8% BoS, F(1,35) = 23.3; P < 0.001; Fig. 4, left].
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The V50, which indicates the velocity at which the transition between the low-/high-threshold boundary on the velocity scale, was lower for the older than for the younger subjects in absolute [17.8 ± 4.3 vs. 23.5 ± 5.1 cm.s–1; F(1,35) = 13.4; P < 0.001] and normalized units [96 ± 24 vs. 121 ± 26% BoS.s–1; F(1,35) = 9.6; P < 0.005, Fig. 4, right]. There was no significant difference in the slopes of the threshold boundaries between groups for the individual subject data [0.27 ± 0.20 vs. 0.36 ± 0.28, F(1,35) = 1.2; P = 0.28].
The older subjects stepped more often than the younger subjects [69 ± 14 versus 40 ± 19% trials; F(1,47) = 38.7; P < 0.001]. This was despite different initial positions, with the older group standing with the CoP 1.6 cm or 8% BoS further back toward the ankles [F(1,47) = 9.4; P < 0.005]. Had they started in the same position, an even larger incidence of stepping would be expected for the older group.
Sensorimotor correlates of stepping
Table 1 shows the correlations of the sensorimotor and neuromuscular measures with TL, TH, and the total number of steps taken for the 124 perturbations. There were no significant correlations with the V50. For each correlation, the Pearson r (left) is the correlation between the stepping parameter and the sensorimotor measure for all subjects. The partial r (right) is the partial correlation coefficient when age is included as an independent factor.
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It can be seen that many of the sensorimotor measures are significantly associated with the threshold measures when the young and old group data are pooled. Of note, vibration sense and visual acuity are associated with all stepping parameters, isokinetic strength and rate of force development are associated with TH, and all measures of strength are associated with the total number of steps. There is a consistent pattern in the signs of the correlation coefficients whereby the worse performances in physiological tests are associated with lower threshold parameters and a greater number of steps. However, none of these associations were present when age was included as a factor (partial r). Thus, although it is apparent that the stepping thresholds are affected by age-related factors, there is no evidence that the sensorimotor factors tested are directly causal in this.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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For the situation of static equilibrium, approximated with the slowest pulls, the threshold boundary is near the foremost point of the BoS. In this condition, the final position of the pelvis approximates accurately the final position of the CoM. A person can balance at or near this point, allowing a margin for his or her ongoing natural body sway, without the CoM falling over the front of the BoS. When the body is moving forward with a significant velocity, it has a kinetic energy that must be overcome by muscular work. This takes time because the reaction time and power output of muscles are finite. Therefore a significant amount of forward sway of the body occurs before the required work is done to arrest this forward movement. If this process brings the body to rest, at or before the forward limit of the BoS, a step need not be taken. If, however, the forward movement takes the CoM past this limit, a step must be taken. Therefore the position threshold for stepping, as determined in this experiment, is considered to be the position of the CoM relative to the ankles that, for any given velocity, will cause the subject to step or not step with equal probability. When the CoM is behind this threshold, not stepping is more likely; when it is in front of the threshold stepping is more likely.
Using this same concept, the stability boundary for stance and thresholds
for stepping during forward perturbations were calculated by Pai and Patton
(1997) from a simple pendulum-
and-foot balance model combined with motion constraints (see also
Patton et al. 1999). In the
present study, this threshold boundary for stepping was determined
experimentally. The stepping threshold boundaries of the two approaches are
considered in the following discussion. They are illustrated for two subjects
in Fig. 5. It is evident that
at low velocities they agree relatively well but an increasing discrepancy
arises as velocity increases. These considerations point out the necessity of
taking into account for future work the segmental strategies used by the
subjects to keep the CoM over the BoS and their influence on the stepping
threshold.
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Threshold boundary
The threshold boundary has two identifiable position plateaus, one at low velocities (TL) and one at high velocities (TH). Between these plateaus, the threshold position and the velocity of the perturbation are inversely related.
LOW-VELOCITY THRESHOLD. TL corresponds to the maximum
amplitude that can be applied at the smallest velocities without inducing a
step. In such quasi-static conditions, the position limit for equilibrium is
the length of the BoS. No matter how slowly it is applied, when the pull
brings the CoM to the limit of the BoS, subjects will have to step. However,
it might be necessary to step before this point is reached. The external
moment produced by gravity progressively increases as the CoM moves forward
and approaches the limit of the BoS. If an equally large internal muscular
moment cannot be produced to maintain equilibrium, a step must be taken before
the CoM reaches the end of the BoS. In young subjects, TL was not
less than the BoS (Figs. 4 and
5), suggesting that this
parameter reflects the anatomical constraints rather than limitation
attributed to ankle strength. Similarly, the forward stability limit modeled
by Pai and Patton (1997) was
unaffected by ankle strengths within the normal range.
TL in younger subjects was 25% larger than the functional BoS
limits measured by having subjects lean forward without lifting the heels or
bending the trunk (King et al.
1994; Schieppati et al.
1994). It is possible that subjects underestimate their limit of
stability during voluntary leaning
(Robinovitch and Cronin 1999).
However, subjects in the present study did not have to maintain the final
position after the pull, thereby removing a period of time in which
superimposed naturally occurring body sway could bring them past the limit of
stability. Furthermore, behavior to avoid stepping was not constrained so that
subjects could raise the heels to extend the BoS forward
(Endo et al. 2002), or flex the
knees and extend the trunk to reduce the forward movement of the CoM
(Iqbal and Pai 2000), or move
their arms to stabilize the body through inertial effects
(Maki and McIlroy 1997).
VELOCITY-DEPENDENT THRESHOLD. At higher velocities, the kinetic energy imparted by the perturbation has to be overcome. Thus the threshold at this range of velocities is now significantly affected by the velocity of the movement and the need to decelerate it before the CoM exceeds the front of the BoS. Thus it is more likely that the amount and rate that muscular torque can be generated at the ankles will play an increasing role in determining the threshold boundary as velocity increases.
HIGH-VELOCITY THRESHOLD. If all of the energy applied by the
perturbation was used to move the whole body forward then the threshold
boundary should not plateau, as we show in this experiment. Instead, it would
be expected to slope downward as velocity increases. Eventually, at a finite
velocity, the threshold should reach zero when the position threshold is at
the ankles, or even become negative when it is behind the ankles. The model of
Pai and Patton (1997) predicts
a continuous inverse relationship between the threshold position to step and
the velocity of the perturbation (Fig.
5). However, the prediction of the dynamic model consistently
underestimated how far in front of the ankles the experimentally derived
threshold was, and this discrepancy became progressively larger as velocity
increased. Thus it appears that the perturbation has different effects on the
forward velocity of the CoM of the modeled and real bodies. In the real
situation, there comes a point where the increase in perturbation velocity has
reduced the perturbation displacement required for threshold to a critically
small level. Above this, further increases in perturbation velocity appear not
to increase the forward velocity of the CoM of the whole body. Thus it appears
that the high velocity threshold is reached when the perturbation displacement
becomes so small that changes in perturbation velocity do not produce
corresponding changes in the movement of the CoM.
Why does this happen? The perturbation was applied at waist level, and unlike a rigid inverted pendulum, the real body is a jointed inverted pendulum so that the trunk does not have to keep up as the hips and legs are pulled forward. Accordingly, the whole-body CoM will be behind that predicted and would more likely remain within the BoS. A strategy that accelerated the top of the body backward could compensate for the forward movement of the lower body. At very small amplitudes the compliance of the soft tissues will absorb a greater proportion of the perturbation energy so that less will be available to accelerate the body. Thus there is a relative discrepancy between the perturbation size and the movement of the CoM, which approaches zero for small perturbations. This filtering of the external perturbations by these largely passive mechanisms is therefore a means by which we normally deal with small disturbances regardless of their velocity or energy.
Physiological correlates
Sensory information could trigger the initiation of a step, much as inputs
from hip (Grillner and Rossignol
1978) and limb extensor muscles
(Duysens and Pearson 1980)
cause a transition from stance to swing phase during walking. Plantar
mechanoreceptors can signal the position of the CoP under the feet during
standing (Kavounoudias et al.
2001; Kennedy and Inglis
2002) and could initiate stepping from the transient associated
with a perturbation. Lower-limb vibration, touch, and proprioceptive
sensibilities indicate the performance of these afferent systems and we
expected that they would be associated with the threshold boundary parameters.
Associations were observed for vibration and touch
(Table 1, Pearson r).
However, the sign of the coefficients does not agree with their direct
physiological reflex functions; poorer performance is associated with stepping
at a lower threshold. The threshold boundary parameters were also associated
with visual acuity, but again, diminished acuity was associated with a lowered
threshold. A similar response of increased stepping frequency to forward
perturbations is observed when the feet are cooled
(Perry et al. 2000). Thus
these behaviors appear to be an adaptation to diminished somatosensory input
such that a step is taken in response to a smaller perturbation.
Muscular strength at the ankles could limit how far forward a subject can lean before he or she loses balance. However, TL was not associated with any measure of ankle strength within the younger or older groups. Therefore the observation that TL is short of the BoS limit for the older group is likely to be related to factors other than muscle strength. There were significant associations of TH with isokinetic strength and the rate of force development, parameters that should be most important for correcting these high-velocity movements. Thus the effects of lower-limb strength on stepping behavior are seen with rapid perturbations, although, like the sensory tests, muscle weakness is associated with a lowered threshold and increased stepping, again indicating a behavioral adaptation.
Simple reaction time is a global measure of sensorimotor integration, central processing, and peripheral factors, so it is surprising that it is only moderately associated with the total steps taken. This again has the same property of poorer performance being associated with more frequent stepping.
Obviously, sensorimotor elements not assessed could also affect the
threshold boundary. For example, patients with bilateral vestibular loss step
more often than controls with rapid perturbations
(Krebs et al. 2000;
Runge et al. 1998) and this
implicates vestibular input in step initiation. However, here again, loss of
vestibular function causes subjects to step more often and lowers the
threshold boundary.
From these observations, we can state as a general principle: Stepping is more likely when there is loss of any peripheral sensory or motor function that is used to step. Peripheral function must be emphasized at this stage because an important variable not tested here, cognitive function, conceivably could behave in the opposite way; that is, poor cognitive function could be associated with a greater stepping threshold.
Age-related changes
The older group of subjects had a lower threshold boundary and stepped twice as often despite adopting a more backward initial position, which is likely to have been a compensation strategy to offset the forthcoming perturbation. Had it been possible to randomize the perturbation directions to negate this strategy, we assume that this group would have taken even more steps than seen in this case because they would have stood closer to the threshold boundary.
TL in the older group fell well short of 100% BoS, the boundary
predicted by Pai and Patton
(1997) for low velocities and
observed in the young group (Fig.
5). For these older subjects, TL was determined by
factors other than BoS limits. The associations of sensorimotor performance
with TL suggest that somatosensory and visual inputs are important
determinants of TL.
TH in the older group was also lower, suggesting a difficulty
responding to rapid perturbations without stepping. This could be expected
from the slower and larger movements of older subjects in response to
support-surface perturbations (Okada et
al. 2001). Associations of TH with isokinetic strength
and the rate of force development suggest that they are determinants of
TH.
Although the boundary was reduced in the older group, the fundamental relationship between amplitude and velocity was preserved, with similar shapes, slopes, and ranges of the threshold boundaries for the younger and older subjects. Thus, although the actual triggering levels adapt with ageing, the way that the CNS integrates the sensory information on which the decision to step is made is preserved.
Across the entire population of younger and older subjects, many sensorimotor factors were significantly associated with TL, TH, and the total number of steps taken but were not present when subject age was removed as a factor (Table 1: compare partial with Pearson coefficients). Therefore it is not possible to claim that the tested physiological factors are directly related to the stepping behavior, given that these factors could be age-related covariates.
Nature of the stepping response
When subjects arrest a forward motion to prevent stepping they allow
spatial and temporal safety margins so that they regain balance well before
the limit of the BoS (Patton et al.,
1999,
2000). Brief training can
modify these safety margins and their variability
(Pavol and Pai 2002) and
stepping can be delayed by 200–300 ms
(Rogers et al. 2003). Thus it
appears that a step is initiated before it is absolutely required to provide
an adequate safety margin for the nonstep response. Only when the safety
margin falls below a critical level is a corrective stepping response
required.
At the higher velocities tested in the present study, the amplitude of the
pull at the threshold boundary had become very small and produced only small
movements of the body. Even among the younger group, but overtly apparent in
the older group, many of the steps taken appeared unnecessary to correct the
postural disturbance arising from the perturbation. This suggests a strategy
change whereby stepping is a preprogrammed response, based on prior learning,
and triggered by any number of factors. In this case, the mere existence of a
perturbation triggers a step rather than the assessment of movement parameters
reflecting the evolving instability that might be used to produce an
appropriately timed, graded, and directed response that will efficiently
arrest the imbalance. It may be for this reason that multiple stepping
(Luchies et al. 1994), altered
lateral stepping (Rogers et al.
2001a), and stepping that further destabilizes posture
(Maki et al. 2000) are
observed in many older people. This is not to say that physiological changes
do not contribute to the altered behavior, but other cognitive influences such
as prior experiences of poor balance, fear of falling, anxiety, and level of
vitality may be more important determinants in the older group. It may be that
the wait-and-see strategy is a luxury afforded only to the young and that the
early step strategy adopted by older people is functionally the optimal
adaptation for diminished sensorimotor performance.
Summary
This study identifies a threshold boundary for triggering protective stepping in response to perturbations applied to the body. This boundary shows a characteristic sigmoidal relationship between position and velocity, with distinct position thresholds for both low- and high-velocity disturbances. This shape is not as predicted from a biomechanical model, with the greatest difference at higher velocities. The differences likely reflect the real-world situation where there is variable transference of the energy of the perturbation into moving the body. A range of sensorimotor physiological variables showed significant associations with the threshold boundary across a large range of subject ages. The nature of these associations was such that poor sensorimotor performance was associated with a position threshold boundary closer to the ankles and therefore more frequent stepping. However, accounting for the effect of age suggested that these variables could be age-related covariates and are not directly responsible for the altered stepping behavior. It appears that stepping is a triggered response based on selected strategy that may change with age.
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DISCLOSURES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests: M. W. Rogers, Department of Physical Therapy and Human Movement Sciences, The Feinberg School of Medicine, Northwestern University, 645 North Michigan Ave., Suite 1100, Chicago, IL 60611 (E-mail: m-rogers{at}northwestern.edu).
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONDISCLOSURESACKNOWLEDGMENTSREFERENCES |
|---|
Capaday C. Neurophysiological methods for studies of the motor system in freely moving human subjects. J Neurosci Methods 74: 201–218, 1997.[ISI][Medline]
De Dominico G and McCloskey DI. Accuracy of voluntary movements at the thumb and elbow joints. Exp Brain Res 65: 471–478, 1997.
Duysens J and Pearson KG. Inhibition of flexor burst generation by loading ankle extensor muscles in walking cats. Brain Res 187: 321–332, 1980.[ISI][Medline]
Endo M,
Ashton-Miller JA, and Alexander NB. Effects of age and gender on toe
flexor muscle strength. J Gerontol A Biol Sci Med Sci
57: M392–M397,
2002.
Grillner S and Rossignol S. On the initiation of the swing phase of locomotion in chronic spinal cats. Brain Res 146: 269–277, 1978.[ISI][Medline]
Horak FB and
Nashner LM. Central programming of postural movements: adaptation to
altered support-surface configurations. J Neurophysiol
55: 1369–1381,
1986.
Iqbal K and Pai YC. Predicted region of stability for balance recovery: motion at the knee joint can improve termination of forward movement. J Biomech 33: 1619–1627, 2000.[ISI][Medline]
Kavounoudias A,
Roll R, and Roll JP. Foot sole and ankle muscle inputs contribute jointly
to human erect posture regulation. J Physiol
532: 869–878,
2001.
Kennedy PM and
Inglis JT. Distribution and behaviour of glabrous cutaneous receptors in
the human foot sole. J Physiol
538: 995–1002,
2002.
Kenshalo DR. Somesthetic sensitivity in young and elderly humans. J Gerontol 41: 632–642, 1986.
King MB, Judge JO, and Wolfson L. Functional base of support decreases with age. J Gerontol 49: M258–M263, 1994.[ISI][Medline]
Krebs DE, Velyvis PH, and Rogers MW. Vestibulopathy and the age effects on protective stepping during unperturbed standing. Motor Control 4: 316–328, 2000.[ISI][Medline]
Lord SR and Castell S. Physical activity program for older persons: effect on balance, strength, neuromuscular control, and reaction time. Arch Phys Med Rehabil 75: 648–652, 1994.[ISI][Medline]
Lord SR, Clark RD, and Webster IW. Postural stability and associated physiological factors in a population of aged persons. J Gerontol 46: M69–M76, 1991.[ISI][Medline]
Luchies CW, Alexander NB, Schultz AB, and Ashton-Miller JA. Stepping responses of young and old adults to postural disturbances: kinematics. J Am Geriatr Soc 42: 506–512, 1994.[ISI][Medline]
Maki BE,
Edmondstone MA, and McIlroy WE. Age-related differences in laterally
directed compensatory stepping behavior. J Gerontol A Biol Sci Med
Sci 55:
M270–M277, 2000.
Maki BE and
McIlroy WE. The role of limb movements in maintaining upright stance: the
"change-in-support" strategy. Phys Ther
77: 488–507,
1997.
McIlroy WE and Maki BE. Task constraints on foot movement and the incidence of compensatory stepping following perturbation of upright stance. Brain Res 616: 30–38, 1993.[ISI][Medline]
Merletti R, Farina D, Gazzoni M, and Schieroni MP. Effect of age on muscle functions investigated with surface electromyography. Muscle Nerve 25: 65–76, 2002.[ISI][Medline]
Nashner LM and McCollum G. The organization of human postural movements: a formal basis and experimental synthesis. Behav Brain Sci 8: 135–172, 1985.
Okada S, Hirakawa K, Takada Y, and Kinoshita H. Age-related differences in postural control in humans in response to a sudden deceleration generated by postural disturbance. Eur J Appl Physiol 85: 10–18, 2001.[ISI][Medline]
Pai YC, Maki BE, Iqbal K, McIlroy WE, and Perry SD. Thresholds for step initiation induced by support-surface translation: a dynamic center-of-mass model provides much better prediction than a static model. J Biomech 33: 387–392, 2000.[ISI][Medline]
Pai YC and Patton J. Center of mass velocity–position predictions for balance control. J Biomech 30: 347–354, 1997.[ISI][Medline]
Pai YC, Rogers MW, Patton J, Cain TD, and Hanke TA. Static versus dynamic predictions of protective stepping following waist-pull perturbations in young and older adults. J Biomech 31: 1111–1118, 1998.[ISI][Medline]
Patton J, Lee WA, and Pai YC. Relative stability improves with experience in a dynamic standing task. Exp Brain Res 135: 117–126, 2000.[ISI][Medline]
Patton J, Pai YC, and Lee WA. Evaluation of a model that determines the stability limits of dynamic balance. Gait Posture 9: 38–49, 1999.[ISI][Medline]
Pavol MJ and Pai YC. Feedforward adaptations are used to compensate for a potential loss of balance. Exp Brain Res 145: 528–538, 2002.[ISI][Medline]
Perry SD, McIlroy WE, and Maki BE. The role of plantar cutaneous mechanoreceptors in the control of compensatory stepping reactions evoked by unpredictable, multi-directional perturbation. Brain Res 877: 401–406, 2000.[ISI][Medline]
Pidcoe PE and Rogers MW. A closed-loop stepper motor waist-pull system for inducing protective stepping in humans. J Biomech 31: 377–381, 1998.[ISI][Medline]
Pitts DG. The effects of aging on selected visual functions: dark adaptation, visual acuity, stereopsis, brightness contrast. In: Aging in Human Visual Functions (Modern Aging Research, vol. 2), edited by Sekuler R, Kline DW, and Dismukes K. New York: A. R. Liss, 1982, p. 131–159.
Robinovitch SN and Cronin T. Perception of postural limits in elderly nursing home and day care participants. J Gerontol A Biol Sci Med Sci 54: B124–B130, 1999.[Abstract]
Rogers MW, Hain TC, Hanke TA, and Janssen I. Stimulus parameters and inertial load: effects on the incidence of protective stepping responses in healthy human subjects. Arch Phys Med Rehabil 77: 363–368, 1996.[ISI][Medline]
Rogers MW,
Hedman LD, Johnson ME, Cain TD, and Hanke TA. Lateral stability during
forward-induced stepping for dynamic balance recovery in young and older
adults. J Gerontol A Biol Sci Med Sci
56: M589–M594,
2001a.
Rogers MW, Hedman LD, Johnson ME, Martinez KM, and Mille ML. Triggering of protective stepping for the control of human balance: age and contextual dependence. Cog Brain Res 16: 192–198, 2003.[Medline]
Rogers MW, Kukulka CG, Brunt D, Cain TD, and Hanke TA. The influence of stimulus cue on the initiation of stepping in young and older adults. Arch Phys Med Rehabil 82: 619–624, 2001b.[ISI][Medline]
Runge CF, Shupert CL, Horak FB, and Zajac FE. Role of vestibular information in initiation of rapid postural responses. Exp Brain Res 122: 403–412, 1998.[ISI][Medline]
Schieppati M, Hugon M, Grasso M, Nardone A, and Galante M. The limits of equilibrium in young and elderly normal subjects and in parkinsonians. Electroencephalogr Clin Neurophysiol 93: 286–298, 1994.[ISI][Medline]
Shumway-Cook A and Woollacott MH. Motor Control: Theory and Practical Applications. Baltimore, MD: Lippincott Williams & Wilkins, 2001.
Skinner HB, Barrack RL, and Cook SD. Age-related decline in proprioception. Clin Orthop 184: 208–211, 1984.
Stelmach GE and Worringham CJ. Sensorimotor deficits related to postural stability. Implications for falling in the elderly. Clin Geriatr Med 1: 679–694, 1985.[Medline]
Vandervoort AA. Aging of the human neuromuscular system. Muscle Nerve 25: 17–25, 2002.[ISI][Medline]
Welford AT. Reaction time, speed of performance, and age. Ann N Y Acad Sci 515: 1–17, 1988.[ISI][Medline]
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