JN Watch the video to learn how APS reaches out to developing nations.
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
 QUICK SEARCH:   [advanced]


     


J Neurophysiol 90: 755-762, 2003; doi:10.1152/jn.01118.2002
0022-3077/03 $5.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (20)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pai, Y.-C.
Right arrow Articles by Pavol, M. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pai, Y.-C.
Right arrow Articles by Pavol, M. J.

Role of Feedforward Control of Movement Stability in Reducing Slip-Related Balance Loss and Falls Among Older Adults

Y.-C. Pai1, J. D. Wening1, E. F. Runtz2, K. Iqbal3 and M. J. Pavol4

1 Department of Physical Therapy, University of Illinois at Chicago, 60612; 2 Department of Physical Therapy and Human Movement Sciences, Northwestern University Medical School, Chicago, Illinois 60611; 3 Department of Systems Engineering, University of Arkansas, Little Rock, Arkansas 72204; 4 Department of Exercise and Sport Science, Oregon State University, Corvallis, Oregon 97331

Submitted 12 December 2002; accepted in final form 5 April 2003


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 ACKNOWLEDGMENTS
 REFERENCES
 
Human upright posture is inherently unstable. To counter the mechanical effect of a large-scale perturbation such as a slip, the CNS can make adaptive adjustments in advance to improve the stability of the body center-of-mass (COM) state (i.e., its velocity and position). Such feedforward control relies on an accurate internal representation of stability limits, which must be a function of anatomical, physiological, and environmental constraints and thus should be computationally deducible based on physical laws of motion. We combined an empirical approach with mathematical modeling to verify the hypothesis that an adaptive improvement in feedforward control of COM stability correlated with a subsequent reduction in balance loss. Forty-one older adults experienced a slip during a sit-to-stand task in a block of slip trials, followed by a block of nonslip trials and a re-slip trial. Their feedforward control of COM stability was quantified as the shortest distance between its state measured at seat-off (slip onset) and the mathematically predicted feasible stability region boundary. With adaptation to repeated slips, older adults were able to exponentially reduce their incidence of falls and backward balance loss, attributable significantly to their improvement in feedforward control of stability. With exposure to slip and nonslip conditions, subjects began to select "optimal" movements that improved stability under both conditions, reducing the reliance on prior knowledge of forthcoming perturbations. These results can be fully accounted for when we assume that an internal representation of the COM stability limits guides the adaptive improvements in the feedforward control of stability.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 ACKNOWLEDGMENTS
 REFERENCES
 
A significant health threat facing the older adult population is their increasing susceptibility to falling with increasing age (Baker and Harvey 1985Go; Holbrook et al. 1984Go; Tinetti et al. 1988Go). Falls are the leading cause of injury-related death or hospitalization in this older population (Baker and Harvey 1985Go). If new and effective clinical training strategies to reduce the risks of falls in the elderly are to be devised, one important requirement is an understanding of the mechanisms whereby the CNS regulates movement and stability (Maki and McIlroy 1996Go; Stelmach and Worringham 1985Go; Woollacott et al. 1999Go).

Because human upright posture is inherently unstable, a primary objective for the CNS must be to prevent falls, achieved first by preventing unintended loss of balance. Loss of balance occurs when the motion state (i.e., instantaneous position and velocity) of the body center-of-mass (COM) with respect to the base of support (BOS) exceeds certain stability limits (Maki 1998Go; Pai 2003Go). It is possible that the CNS can integrate afferent inputs of different origins to monitor and update the current COM state and readily compare it with a corresponding internal representation of these stability limits. Adaptive refinement of the internal representation of postural stability to account for real or potential perturbation may be required to improve the CNS's ability to prevent balance loss. The CNS can then select and execute an appropriate action in a feedforward control manner, to counter the perturbation and to avert any unintended balance loss.

It is logical to postulate that, relying on prior experience and memory, the CNS must be able to quantify the likelihood of balance loss. This ability would likely require the mapping of stability limits, possibly in terms of a feasible stability region in the COM state space (Pai and Patton 1997Go). Outside of this region, the tasks of movement termination and balance recovery for upright standing can never be simultaneously successful. Theoretically, these stability limits can also be deduced mathematically based on assumed stability criteria, the dynamics of the body, anatomical and physiological limitations, and environmental constraints. For its verification and the demonstration of the potential of its practical application, this concept can be applied to theorize the prevention of slip-related falls. It is predicted that a backward balance loss can be avoided through the use of feedforward control to improve stability at the onset of a slip. Specifically, one can increase the forward COM velocity and/or anteriorly shift the COM position to achieve this objective (Pai and Iqbal 1999Go). The same mathematical model simulation predicts the existence of a set of "optimal" movement strategies that satisfy the constraints associated with avoiding a loss of balance under both slip and nonslip conditions (Pai and Iqbal 1999Go). Such movement options are optimal because they simultaneously reduce the likelihood of a balance loss under both possible conditions when facing the uncertainty that a slip may or may not occur. Thus they can lessen the reliance of the CNS on detailed and accurate knowledge of a forthcoming balance perturbation.

Recent empirical evidence showed that fall incidence in older adults decreased with repeated exposure to slipping and nonslipping conditions (Pavol et al. 2002bGo) and that this decrease was associated with anticipatory (proactive) adjustments to COM state (Pavol et al. 2002d). It is still unclear, however, the extent to which stability at slip onset, as quantified through the feasible stability region concept, can actually explain reductions in backward balance loss and fall incidence. Existence of such a relationship would lend support to the feasible stability region as a conceptual model of the hypothesized CNS internal representation of stability limits, thereby supporting its application to fall prevention. Further, this relationship would support the theory that the internal representation of stability limits can be rapidly refined (i.e., updated or modified) through repeated perturbation exposure.

The purpose of this study was to verify this concept of adaptive feedforward control of movement (dynamic) stability by testing three specific hypotheses. First, movement stability can be improved among older adults through repeated slip exposure, such that the improvement correlates with a reduction in the likelihood of backward balance loss that, in turn, should be associated with a reduction in fall incidence. Conversely, a reduction in movement stability against forward balance loss due to overcompensation will correlate with an elevated risk of forward balance loss, which can again be reduced with an adaptive improvement in movement stability. Last, the predicted optimal movement strategies to counter the uncertainty of a slip are attainable, such that movement stability is achieved under both slip and nonslip conditions and the likelihood of both forward and backward balance loss is reduced.


    METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 ACKNOWLEDGMENTS
 REFERENCES
 
Mathematical derivation of feasible stability region

The feasible stability region is defined as all combinations of COM anteroposterior position and velocity for which a loss of balance is preventable. Loss of balance for a given initial position and velocity occurs when this velocity of the COM relative to the BOS cannot be reduced to zero within the existing BOS limits, but only with a change in the BOS. To search for the boundaries of the feasible stability region, we used a two-link model (Fig. 1a) with an optimization control loop (Fig. 1c). One model segment represented the symmetrical placement of the feet and the second segment represented the rest of the body. The equations of motion for this two-link model with two degrees-of-freedom under slipping conditions (Pai and Iqbal 1999Go) are listed in Fig. 1b.



View larger version (23K):
[in this window]
[in a new window]
 
FIG. 1. A: free body diagram of the 2-link (feet + rest-of-body) inverted pendulum model of the human body (left), and definition of variables (right). B: the equations of motion, where m is the mass of the body minus feet; mf, the mass of the feet; r, the length to the pendulum mass center; {theta}, the angular position of the body segment; x, the displacement of the base of support; {tau}, the ankle joint moment; Fx, the horizontal component of the ground reaction force; Fy, the vertical component of the ground reaction force acting at the center of pressure (COP); µ, the coefficient of friction; g, the acceleration due to gravity; and c: a schematic representation of the model simulation and optimization process.

 

Forward dynamic solutions for these equations were derived by numerical integration using a fourth-order Runge-Kutta method, where initial conditions were the initial body state and joint moment estimates. The model was controlled through joint moments, which were parameterized as a mathematical function exhibiting sigmoid variation with time. The outputs of the simulation included time-histories of the horizontal and vertical components of the ground reaction force and the COM position and velocity (Pai and Iqbal 1999Go).

Optimization entailed an iterative process of movement simulation, evaluation of the cost function from the simulation results, and updating the model inputs based on the method of steepest descent (Pai and Iqbal 1999Go). The task objectives of a successful movement termination were quantified through a cost function. It incorporated mathematical expressions representing the desired final state of the model, the anatomical (e.g., joint range of motion) and physiological (e.g., muscle strength) limitations, the environmental constraints (e.g., characteristics of the ground reaction force), and the limits on the parameters that defined the joint moment profiles. The maximum horizontal ground reaction force component was determined by the coefficient of friction.

The solution derived from the simulation and optimization process determined, for a given COM position, the minimum initial COM velocity at which a backward loss of balance could be avoided. This process was repeated at other COM positions and for forward loss of balance. Polynomial interpolation between solutions was used to outline the boundary of the feasible stability region. Separate feasible stability regions were determined for slipping and nonslipping conditions, using the corresponding coefficients of friction.

Subjects

Following approval by the Institutional Review Board, 41 healthy older adults (21 women) gave written informed consent and were paid to participate. They were ambulatory, community-dwelling individuals >=65 yr of age (mean ± SD age: 73 ± 5 yr; height: 1.69 ± 0.09 m; mass: 79 ± 14 kg). Subjects were screened for the following exclusionary factors: neurological, musculoskeletal, cardiopulmonary, and other systemic disorders, selected drug usage (e.g., tranquilizers), cognitive impairment, poor mobility, and orthostatic hypotension. Calcaneal bone mineral density was assessed and individuals with bone loss (i.e., osteopenic or osteoporotic) were excluded to reduce the risk of fracture on an actual, harness-arrested fall.

Experimental protocol and data collection

Slips were induced during a sit-to-stand movement using a protocol that has been detailed previously (Pavol et al. 2002bGo). Trials began with subjects sitting on a stool in a standardized position such that the heels were aligned, knees flexed to 100° from the anatomic position, and ankles at 10° dorsiflexion. After four regular sit-to-stand trials, a block of five consecutive slip trials (trials S-1 through S-5) was introduced without warning. This was followed by a block of three nonslip trials (trials NS-1 through NS-3). Subjects were then exposed to another slip trial (the re-slip trial, RS-1). Subjects were originally informed that they would initially be performing sit-to-stand trials and that "later on" a slip would take place. No practice was given, and the exact trial, timing, and mechanisms of the slip were not provided. After the first slip, subjects were informed that a slip "may or may not occur" during subsequent trials.

Slips were induced using two low-friction platforms (dimensions: 31 x 29 cm, friction coefficient: 0.02) placed side-by-side such that each foot rested on its own platform. Slips were initiated by a computer-controlled release of the low-friction platforms when the weight on the seat fell below 10% of body weight as measured by a force plate (AMTI, Newton, MA). As a result of rapid unloading, coupled with sampling and mechanical delays, the load applied to the seat by the subject reached zero 0.013 ± 0.010 s prior to movement of the sliding platforms. On release, the platforms moved forward freely and independently. After a maximum travel of 24 cm, the platform locked in the forward position. At least one platform traveled the maximum distance in 99.2% of all slips by all subjects. The mean duration for the first slip was 0.43 ± 0.10 s, with the platform reaching a mean peak velocity and acceleration of 0.86 ± 0.17 m/s and 8.18 ± 2.24 m/s2, respectively. Figure 2 shows a time history of the COM and BOS position and velocity, as well as the vertical ground reaction force for a representative slip. Subjects wore a full-body safety harness attached at the shoulders to a ceiling-mounted support by a pair of shock-absorbing dynamic ropes, typically used for fall protection in rock climbing. Rope lengths were adjusted so the knees could not touch the flooring. A load cell monitored the force exerted on the ropes.



View larger version (33K):
[in this window]
[in a new window]
 
FIG. 2. A sample sit-to-stand trial with a slip that resulted in a backward balance loss, a left backward step, and a fall. Time histories of the absolute position (top) and velocity (middle) of the body center of mass (COM, solid line), and base of support (BOS, dashed line) are presented. The BOS kinematics are derived based on the adjusted right heel which remains stationary with respect to the sliding platform during stance regardless whether there is a heel raise. Positive or increasing values represent velocity or position in the anterior direction, respectively, and negative or decreasing values in the posterior direction. Also included is the time history of the vertical force (bottom) applied to the seat (solid line) and by the right foot (dashed line). The vertical lines mark the time of slip onset (Onset; the same instant corresponding to the triangle in Fig. 3b), liftoff (LO), and touchdown (TD) of the stepping foot, and the time at which harness support started (Fall). The slip begins just as the force on the seat decreases to zero.

 



View larger version (35K):
[in this window]
[in a new window]
 
FIG. 3. A: the feasible stability region (FSR) for slipping (area enclosed by thick line) and nonslip conditions (area enclosed by thin line), modified based on Fig. 4 in Pai and Iqbal (1999Go). Notably, as shown by the shaded region, there exists a set of center-of-mass states that is contained in the feasible stability regions for both nonslipping and slipping conditions. These represent optimal movement strategies, for which a loss of balance can be avoided, regardless of whether or not a slip occurs. B: examples of the center of mass state (velocity, COM, and position, XCOM) trajectories with reference to the mathematically predicted regions for backward loss of balance under slip conditions ("Backward LOB-S") and for forward loss of balance under nonslip conditions ("Forward LOB-NS"). Shown is a typical first slip trial (S-1, thick dotted line), first nonslip trial (NS-1, thick solid line), third nonslip trial (NS-3, thin solid line), and the re-slip trial (RS-1, thin dotted line). A triangle marks the COM state at the time of seat-off, and a circle marks the COM state at the end of balance recovery (NS-3, RS-1) or at compensatory step liftoff (S-1, NS-1). In support of the model prediction, the trajectory of S-1 traversed into the predicted backward balance loss region prior to a fall or step liftoff for all subjects, and all subjects lost balance. Also, the trajectory of NS-1 traversed into the forward balance loss region prior to step liftoff for all subjects who experienced forward balance loss. The shaded region (the same as in A) is optimal for avoiding a balance loss whether or not a slip occurs (NS-3, RS-1 trajectories both remain within the region). The COM anterior position and forward velocity are expressed relative to the rear of the BOS and were converted into dimensionless variables as a fraction of lBOS and , respectively, where lBOS is the length of the base of support, g is the acceleration due to gravity, and h is the body height.

 
The kinematics of markers attached to the bilateral upper and lower extremities, torso, and platforms were recorded by a motion capture system at 60 Hz (Peak Performance, Englewood, CO). Marker paths were low-pass-filtered at marker specific cut-off frequencies ranging from 4.5 to 9 Hz using a recursive, fourth-order Butterworth filter. Locations of joint centers, heels, and toes were computed from the marker paths. These data were used to determine the anterior position and forward velocity of the COM with respect to the rear of the BOS (i.e., the heel of the posterior foot in ground contact) for each trial based on anthropometric data (Pavol et al. 2002aGo). The COM position and velocity were expressed as dimensionless fractions of lBOS and (McMahon 1984Go), respectively, where lBOS is the length of the base of support, g is the acceleration due to gravity, and h is the body height.

Analysis and statistics

A fall was defined based on the vertical descent of the hips after slip onset, occurring if the midpoint between the bilateral hip joint centers descended below 5% body height above its initial seated height. Other trials were considered harness-affected if the average force on the ropes exceeded 4.5% body weight over any 1-s period. The remaining trials were considered recoveries. Classification thresholds were determined post-hoc from clear divisions in the data distributions and were confirmed by the inspection of video recording images.

A balance loss was determined to have occurred if a subject stepped to regain balance, that is, took a step that extended the BOS in the direction of stepping. The direction of the first such step was considered the direction of balance loss. If a subject recovered and did not step to regain balance, no balance loss occurred. For fall or harness-affected trials in which the subject did not step to regain balance, the direction of balance loss was determined from the position of the COM at the defined time of fall or start of harness effects, respectively. A COM position anterior to the more anterior toe or posterior to the more posterior heel corresponded to a forward or backward balance loss, respectively. Occasionally, due to equipment malfunction or experimenter error data were lost or a slip did not occur as intended. Six such trials were excluded from analysis.

The stability of a movement could be assessed by comparing the corresponding COM state trajectory to the mathematically derived feasible stability region boundaries for forward or backward balance loss under slip or nonslip conditions (Fig. 3). At seat-off, the stability against backward balance loss under slip conditions was quantified as the shortest distance between the instantaneous COM state and the boundary for backward balance loss under slip conditions (d in Fig. 4). Because the risks of forward and backward balance loss exist simultaneously, when expressed as a fraction of the corresponding width of the feasible stability region this measure also quantifies the stability against forward balance loss (Fig. 4). The stability under nonslip conditions at seat-off was computed similarly, based on the corresponding feasible stability region for nonslip conditions.



View larger version (71K):
[in this window]
[in a new window]
 
FIG. 4. A schematic definition of the stability measure inside of the feasible stability region (open region) that separates the forward ("Forward LOB-S", shaded in gray) and the backward ("Backward LOB-S", shaded in gray) balance loss regions mathematically derived for slip conditions in the center of mass (COM) state space. Stability at seat-off is measured by the shortest inwardly directed distance (d) to the COM state at seat-off (at location s with triangle) from the backward loss of balance boundary of the feasible stability region. This distance is expressed as a fraction of the width of the feasible stability region measured along the inwardly directed position vector of s from the backward balance loss boundary. In this convention, an unstable COM state for backward balance loss is <0, and an unstable state for forward balance loss is >1. A similar measure of stability can be derived for nonslip conditions from the corresponding feasible stability region.

 

Our model predicts that, based on anatomical and physiological limitations and environmental constraints, a backward loss of balance must occur for COM states outside the corresponding boundary of the feasible stability region. Thus values <0 or >1 correspond to a predicted backward or forward balance loss, respectively. Backward balance loss should not occur when the stability measure is above the predicted threshold for backward balance loss (0 <= d), because the COM forward momentum is sufficient to carry the COM forward from its current position to catch up with the BOS if the motor response (i.e., joint moments) is appropriate. Our rationale is that the farther inside the feasible stability region and away from the backward balance loss boundary the COM state is at slip onset, the greater the allowable deviations in the subsequent motor response, hence the greater the likelihood of avoiding a backward loss of balance through the response employed. Greater values of the above-defined stability measure are therefore taken to reflect greater stability against subsequent backward balance loss. An identical rationale is applicable to forward balance loss, although the numerical relationship between stability and the convention of the defined measure becomes both reversed and centered at 1 instead of 0. Values of the stability measure below the threshold for forward balance loss (d <= 1) reflect an increase in stability relative to forward loss of balance. A COM stability at slip onset that is >1 will be very favorable for avoiding a backward loss of balance, but will unavoidably result in a forward loss of balance.

An adaptive effect across trials of repeated slip exposure on reducing the incidence of backward balance loss and falls (vs. recoveries) was tested for the slipping block using a nonlinear (exponential) regression model. Logistic regression analyses determined the relationships between the mathematically predicted stability at seat-off and the corresponding probability of balance loss under the same conditions. Data from all slip trials (S-1 through S-5, RS-1) and from all trials in the subsequent nonslip block (NS-1 through NS-3) were pooled across subjects for the analysis of backward and forward balance loss, respectively. The goodness of fit for the logistic regression models was assessed by expanding each model with higher order (quadratic and cubic) terms and evaluating the difference in the –2 log likelihood between the original (reduced) model and the expanded (full) model. If the reduced model is sufficient to explain the data, the –2 log likelihood of the logistic regression will not improve significantly on adding other terms (i.e., {alpha} > 0.05 on a {chi}2 distribution). To evaluate the predictive ability of these relationships, the probable balance loss outcome for each trial of each subject was estimated from the calculated COM stability at seat-off, based on the results of the corresponding logistic regression equation (i.e., balance loss occurs when probability >=0.5). This estimated percentage of subjects who lost balance in each trial was then correlated with the percentage of those who actually experienced balance loss in the same trial.

A one-way repeated-measures ANOVA was used to test for adaptive changes across trials in the predicted COM stability under slip conditions at seat-off. All slip trials were included in this test, along with trials NS-1, NS-3, and the trial preceding S-1 (STS). The nonslip trials were included to confirm feedforward adaptations in stability. A similar analysis was performed to test for adaptive changes in the predicted stability under nonslip conditions at seat-off. Post-hoc paired t-tests with Bonferroni corrections were used to identify trial-to-trial adaptive effects by examining differences between consecutive trials, as well as cross-block adaptive differences between S-1 and RS-1, between NS-1 and RS-1, and finally between STS and each of NS-1, NS-3, and RS-1.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 ACKNOWLEDGMENTS
 REFERENCES
 
Adaptation to slips

The incidence of both backward balance loss and backward falls among older adults decreased exponentially with repeated slip exposure (Fig. 5). The incidence of balance loss was greater than the incidence of falls initially (P < 0.01) and decreased at a slower rate (exponential rate constant of –0.48/trial vs. –1.07/trial, P < 0.01). A balance loss was a necessary but not a sufficient condition for an actual harness-arrested fall.



View larger version (23K):
[in this window]
[in a new window]
 
FIG. 5. Backward balance loss and fall incidence decreased exponentially with repeated slip exposure in the block of slip trials. The corresponding best-fit joint exponential relationship (i = 0 for balance loss and 1 for fall in the displayed equation), identified through nonlinear regression, explained 97.9% of the variance in the percentage of balance loss and falls (P < 0.01 for all parameters). The rate of incidence decline was almost twice as fast for falls as for balance loss (exponential rate constants of –1.07/trial and –0.48/trial, respectively).

 

An increase in the predicted stability under slip conditions at seat-off correlated with a decrease in the corresponding probability of backward balance loss. There was a significant (P < 0.01) logistic relationship between predicted stability at seat-off and backward balance loss under slip conditions (Fig. 6a). This relationship was sufficient to explain the data, as the addition of higher order terms did not significantly improve the model (P = 0.97). A strong correlation (r = 0.979, P < 0.01) existed between the estimated (based on the logistic regression equation) and actual incidence of backward balance loss across trials (Fig. 6b). The decreased incidence of backward balance loss with repeated slip exposure was related to an increase in stability against backward balance loss at slip onset (i.e., an increase in the value of the predicted stability measure in Fig. 7a). There was significant improvement (P < 0.01) in stability against backward balance loss under slip conditions at seat-off between trials S-1 and S-2 and between trials S-2 and S-3 (Fig. 7a), but no further change for the remainder of the slip block (P > 0.05).



View larger version (16K):
[in this window]
[in a new window]
 
FIG. 6. A: logistic regression model of the relationship between the mathematically predicted stability under slip conditions at seat-off and the probability of backward balance loss, derived from all slip trials (S-1 through S-5, RS-1, n = 241). The broken vertical line indicates the computed threshold for balance loss derived from the logistic regression equation (i.e., the value of x when y = 0.5). B: percentage of backward balance loss in each of the slip trials as estimated from the logistic regression-based balance loss threshold is strongly correlated (r2 = 0.957, P < 0.01) with the actual percentage of backward balance loss.

 


View larger version (17K):
[in this window]
[in a new window]
 
FIG. 7. A: means and SD of the mathematically predicted stability under slip conditions at seat-off for the slip block trials (S-1 to S-5) and the re-slip trial (RS-1). The preceding regular sit-to-stand trial (STS) and the first and third nonslip trials (NS-1, NS-3) are included for contrast. B: mean and SD of the mathematically predicted stability under nonslip conditions at seat-off for the nonslip block trials (NS-1 to NS-3). Trials S-5 and RS-1 are included for contrast. Larger values of predicted stability in (a) and (b) are interpreted as increased stability against backward balance loss and decreased stability against forward balance loss. Significant differences with respect to the preceding trial (solid line) or cross block trial (broken line) are indicated (* = P < 0.01).

 

Overcompensation and adaptation

An elevated risk for forward balance loss accompanied the adaptation to repeated slips, due to an equivalent of overcompensation under nonslip conditions. As evidence thereof, the stability at seat-off against forward balance loss under nonslip conditions was significantly less (P < 0.01) in trial NS-1 than in STS (i.e., the value of the predicted stability measure in Fig. 7b was greater), while the stability was not different for NS-1 and the preceding S-5 (P > 0.05).

After only a single nonslip trial (NS-1), subjects adapted to reverse the overcompensation by improving stability against forward balance loss under the nonslip condition (i.e., a significant decrease in the value of the stability measure in Fig. 7b, P < 0.01). This effect was retained with no further changes in stability during the remainder of the nonslip block (from NS-2 to NS-3) and the re-slip trial (RS-1) (P > 0.05). Again, a significant (P < 0.01) logistic relationship existed between predicted stability at seat-off and forward balance loss under nonslip conditions (Fig. 8a). This relationship was sufficient to explain the data, as the addition of higher order terms did not significantly improve the model (P = 0.79). A strong correlation (r = 0.978, P < 0.01) between the estimated and actual incidence of forward balance loss across trials (Fig. 8b) also supports the strength of the model.



View larger version (15K):
[in this window]
[in a new window]
 
FIG. 8. A: logistic regression model of the relationship between the mathematically predicted stability under nonslip conditions at seat-off and the probability of forward balance loss, derived from all trials of the nonslip block (NS-1 through NS-3, n = 123). The broken vertical line indicates the computed threshold for balance loss derived from the logistic regression equation (i.e., the value of x when y = 0.5). B: percentage of forward balance loss in each of trials NS-1 through NS-3 of the nonslip block as estimated based on the logistic relationship is strongly correlated (r2 = 0.972, P < 0.01) with the actual percentage of forward balance loss.

 

Optimal movement strategies

With exposure to slip and nonslip conditions, subjects began to adapt toward an optimal movement strategy that allowed a balance loss to be avoided under both conditions. Such adaptation is demonstrated by the convergence of the COM state at seat-off toward the midline between the loss of balance regions in Fig. 3, a and b. It is important to note that subjects did not return to the regular sit-to-stand behavior that they exhibited prior to the first slip exposure. The adapted subjects were significantly more stable at seat-off against backward balance loss under slip conditions (RS-1 vs. STS in Fig. 7a) than during the regular STS trial (P < 0.01).

As further demonstration of this optimal movement strategy, the predicted stability at seat-off of the re-slip against a backward balance loss under slip conditions was significantly greater (P < 0.01) than on the first slip (cf. S-1 vs. RS-1 in Fig. 7a). Meanwhile, the predicted stability at seat-off of the re-slip against a forward balance loss under nonslip conditions was greater (P < 0.01) than on the first nonslip trial (cf. NS-1 vs. RS-1 in Fig. 7b). Furthermore, 12 of 38 (31%) older adults analyzed avoided a balance loss in both RS-1 and its preceding NS-3 (an example shown in Fig. 3b) with no differences in predicted stability at seat-off between these trials (P > 0.05 in Fig. 7, a and b). This represents a substantial improvement as compared with 100% backward balance losses in trial S-1 and 88% forward balance losses in NS-1. The reductions in balance loss were accompanied by a substantial decrease in fall incidence from 73% in S-1 to only 20% in RS-1.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 ACKNOWLEDGMENTS
 REFERENCES
 
Implication, limitations, and predictability

The experimental results can be fully accounted for if we assume that probability of balance loss and dynamic stability limits under slip and nonslip conditions are predictable mathematically, and perhaps neurophysiologically, and that the feedforward stability control that the CNS employs must require an internal representation of these limits. First, an improvement associated with adaptation to repeated slip exposure in the mathematically predicted stability at seat-off (slip onset) correlated significantly with a reduction in backward balance loss after seat-off during subsequent recovery response to the slip. Second, an overcompensation-related reduction in stability against forward balance loss was associated with an elevated risk for forward balance loss when slips stopped occurring. A subsequent improvement in stability against forward balance loss at seat-off correlated significantly with a reduction in forward balance loss in the nonslip trials. Finally, the predicted optimal movement options began to emerge with alternate exposure to slip and nonslip conditions. Without receiving any explicit or implicit instruction on how to adapt, the older adults began to converge their COM state at seat-off toward the optimal region as predicted mathematically. This adaptive process therefore led to a reduced incidence of balance loss, regardless of whether or not a slip occurred.

The persistence of these proactive, feedforward control adaptations and of any underlying refinements in an internal representation of stability limits is presently unknown, nor is it known whether such refinements in stability limits will transfer to altered feedforward control and a reduced likelihood of balance loss during other tasks. Nevertheless, because of the relatively rare real-life occurrence of slips during a sit-to-stand, the present paradigm provided a unique opportunity to observe older adults' natural process of adaptation with minimal bias from prior experience.

Despite the insights gained, limitations exist in the present analyses of stability. The feasible stability regions were based on a simplified representation of the body by a two-link model and the assumption of an infinite slip distance. Motion at the knees and hips can expand the feasible stability region (Iqbal and Pai 2000Go), while termination of foot movement after a finite slip aids in preventing a backward balance loss, also altering the feasible stability region.

It was further assumed that subjects stepped strictly from necessity because of balance loss. A previous study found that 17% of forward steps and 41% of backward steps following a postural perturbation may have been unnecessary (Pai et al. 2000Go). Such inherent error in identifying balance loss might explain the consistent overestimation of balance losses as compared with the number of actual balance losses. This overestimation resulted in a notable deviation of the regression equations in Figs. 6b and 8b from lines of unity. Initiating a step while inside the feasible stability region may reflect a reflexive response, ill-perceived needs, fall-related fear or anxiety, lack of explicit instruction not to step, or simply a choice with no obvious reasons. The feasible stability region is mathematically established by ruling out systematically all the impossibilities (i.e., violations of the constraints) outside the region, rather than proving the possibilities inside it.

In fact, when the COM state trajectory travels outside of the feasible stability region (stability measure <0 or >1), the deterministic models (Iqbal and Pai 2000Go; Pai and Iqbal 1999Go; Pai and Patton 1997Go) are robust in predicting the triggering of a step, with success rates ranging from 93 to 100% (Pai et al. 1998Go, 2000Go; Patton et al. 1999Go). In the first slip trial of this study, each of the 41 subjects' COM state traversed into the predicted backward balance loss region after slip onset, as shown in Fig. 3b, and each subject stepped and/or fell. Similar backward steps occurred in each of the subsequent trials in which the COM state trajectory traversed into the predicted backward balance loss region. Furthermore, in the nonslip trials, those whose COM state traversed into the corresponding forward balance loss region all initiated a forward step (Fig. 3b).

Proactive and reactive strategies of balance control

The event of seat-off during a regular sit-to-stand task represents a self-induced balance perturbation, as the body becomes statically unstable at the instant of seat-off. Proactive use of feedforward control to counter this self-induced perturbation and achieve standing balance relies on coordination of ground reaction forces exerted at the buttocks and feet before seat-off (Hirschfeld et al. 1999Go). During a perturbed sit-to-stand task, proactive use (before slip onset) of feedforward control to improve movement stability must also rely on accurate coordination of ground reaction forces. The present experimental protocol required the CNS to accommodate a change in surface friction and to reconcile the stability limits associated with slip and nonslip conditions. The results indicate that the CNS achieved this, at least in part, through altering its feedforward control of the sit-to-stand task in a continuous adaptive process. The consistency between these adaptations and the conceptual framework of the feasible stability region suggests that the present mathematical computational approach must mimic, in some way, the function of the CNS. It thus seems likely that the observed adaptations in feedforward control were guided by an updated or modified internal representation of the stability region that reflected the perceived changes in external constraints (Witney et al. 2001Go; Wolpert and Ghahramani 2000Go; Wolpert et al. 1995Go).

Because of its proactive nature, feedforward control can successfully reduce or even eliminate the need for a reactive stepping response, as has been shown in this study and others (Pavol and Pai 2002Go). The importance of the reactive response (following the onset of a slip), however, should not be neglected. Successful recovery can rely on an effective reactive response, in which a feedback control can play a large role. A wide range of reactive strategies commonly employed to restore balance includes grasping (Holliday et al. 1990Go; Luchies et al. 1994Go), ankle and hip motion (ankle/hip strategy) (Horak 1992Go; Horak and Nashner 1986Go), and compensatory stepping (Maki and McIlroy 1997Go). The stepping response has a unique and irreplaceable importance in fall prevention, particularly following large disturbances of balance. Arguably, proactive adaptations to movement stability represent a first line of defense against falling, whereas reactive responses represent a second line of defense; both play an important role.

Aging and adaptability in balance control

The present older adults were more likely than young to fall on initial exposure to a slip during a sit-to-stand (Pavol et al. 2002bGo), yet the mechanisms of falling were similar (Pavol et al. 2002c,d). Subsequently, on repeated slip exposure, older and young adults clearly evidenced similar patterns of adaptive changes in the feedforward control of the COM state trajectory, influencing the likelihood of both balance loss and falls (Pavol and Pai 2002Go; Pavol et al. 2002d). Adaptive feedforward control of stability based on a continuously updated internal model thus appears to be used by old and young alike. Evidence suggests, however, that the effective size (quantifiable by the triggering threshold of a stepping response) of the feasible stability region decreases with older age, and with it the magnitude of the adaptive changes in feedforward control (Pavol et al. 2002d).

The results indicated that adaptation of the feedforward control began immediately on a change in conditions and that a steady-state adaptation was attained in two trials or less. Such rapid adaptive behavior in feedforward control has also been demonstrated in other activities (Lang and Bastian 1999Go; Marigold and Patla 2001Go; Owings et al. 2001Go; Scheidt et al. 2001Go). Similarly, a person's reactive response can be rapidly modulated to better restore balance and upright posture (Buchanan and Horak 1999Go; Marigold and Patla 2001Go; Nashner 1976Go) or to provide better weight support from the slipping limb during the recovery (Pavol et al. 2002d). The fact that fall incidence decreased at a faster rate than the reduction in balance loss is noteworthy. It suggests that slip-related falls decreased, not only because older adults proactively improved their movement stability at slip onset (Fig. 7), but also because they rapidly learned to adaptively improve their reactive response so that the proportion of balance losses resulting in falls decreases (Fig. 5). Such adaptive improvements in reactive response have, in fact, been reported and are similar in older and young adults (Pavol et al. 2002d).

Slips contribute to 25% of falls by older adults (Hausdorff et al. 1997Go) and often lead to a backward fall incident (Topper et al. 1993Go) that predisposes the faller to hip fracture (Smeesters et al. 2001Go). It is promising that repeated slip exposure under a protective environment appeared to be effective in facilitating an update or modification of the internal representation of stability limits and in inducing improvements in the feedforward control of movement stability, including the adoption of optimal movement strategies. With such optimal movement strategies, a balance loss can be avoided regardless of whether or not a slip occurs, thereby reducing the reliance on precise or detailed knowledge (which is frequently absent in real-life situations) of forthcoming balance perturbations. It is conceivable that older adults could learn to proactively adopt a similar optimal movement strategy in response to generalized environmental cues, such as a general knowledge of icy weather conditions or a wet floor surface, thereby averting unintended balance losses through feedforward control of stability without sacrificing their mobility.


    DISCLOSURES
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 ACKNOWLEDGMENTS
 REFERENCES
 
This work was funded by National Institutes on Aging R01AG-16727 and the Whitaker Foundation.


    ACKNOWLEDGMENTS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 ACKNOWLEDGMENTS
 REFERENCES
 
We thank the Buehler Center on Aging, Drs. Folasade Ojo, Beatrice Edwards, and N. Francis, for assisting in subject recruitment and screening. The authors also thank Drs. Joanna Q. Wang for statistical consultation and Ziaul Hasan for insightful suggestions, T. Bui for fabricating the platforms, and G. Gagnon, S. Iannaccone, and K. Irwin for assisting in data collection and analysis. The experiments were conducted in the Department of Physical Therapy and Human Movement Sciences at Northwestern University Medical School.


    FOOTNOTES
 
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Address for reprint requests: Y.-C. Pai, Department of Physical Therapy, University of Illinois at Chicago, 1919 West Taylor St., Room 426 (M/C 898), Chicago, Illinois 60612 (E-mail: cpai{at}uic.edu).


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 DISCLOSURES
 ACKNOWLEDGMENTS
 REFERENCES
 
Baker SP and Harvey AH. Fall injuries in the elderly. Clin Geriatr Med 1: 501–512, 1985.[Medline]

Buchanan JJ and Horak FB. Emergence of postural patterns as a function of vision and translation frequency. J Neurophysiol 81: 2325–2339, 1999.[Abstract/Free Full Text]

Hausdorff JM, Edelberg HK, Mitchell SL, Goldberger AL, and Wei JY. Increased gait unsteadiness in community-dwelling elderly fallers. Arch Phys Med Rehabil 78: 278–283, 1997.[ISI][Medline]

Hirschfeld H, Thorsteinsdottir M, and Olsson E. Coordinated ground forces exerted by buttocks and feet are adequately programmed for weight transfer during sit-to-stand. J Neurophysiol 82: 3021–3029, 1999.[Abstract/Free Full Text]

Holbrook TL, Grazier K, Kelsey JL, and Stautter RN. The frequency of occurrence, impact, and cost of selected musculoskeletal conditions in the United States. AAOS 1984.

Holliday PJ, Fernie GR, Gryfe CI, and Griggs GT. Video recording of spontaneous falls of the elderly. In: Slips, Stumbles, and Falls: Pedestrian Footwear and Surfaces (ASTM STP 1103), edited by Gray BE. Philadelphia: American Society for Testing and Materials, 1990, p. 7–16.

Horak FB. Effects of neurological disorders on postural movement strategies in the elderly. In: Falls, Balance, and Gait Disorders in the Elderly, edited by Vellas B, Toupet M, Rubenstein L, Albarede JL, and Christen Y. Paris: Elsevier, 1992, p. 137–151.

Horak FB and Nashner LM. Central programming of postural movements: adaptation to altered support-surface configurations. J Neurophysiol 55: 1369–1381, 1986.[Abstract/Free Full Text]

Iqbal K and Pai Y-C. 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]

Lang CE and Bastian AJ. Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol 82: 2108–2119, 1999.[Abstract/Free Full Text]

Luchies CW, Alexander NB, Schultz AB, and Ashton-Miller J. Stepping responses of young and old adults to postural disturbances: kinematics. J Am Geriat Soc 42: 506–512, 1994.[ISI][Medline]

Maki BE. Is center of mass a controlled parameter? Satellite to the Annual Meeting of the Society for Neuroscience (Identifying Control Mechanisms for Postural Behaviors), Los Angeles, 1998.

Maki BE and McIlroy WE. Postural control in the older adult. Clin Geriat Med 12: 635–658, 1996.[ISI][Medline]

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.[Abstract/Free Full Text]

Marigold DS and Patla A. Strategies for dynamic stability during locomotion on a slippery surface: effects of prior experience and knowledge. J Neurophysiol 88: 339–353, 2001.

McMahon TA. Muscles, Reflexes, and Locomotion. Princeton, NJ: Princeton Univ. Press, 1984.

Nashner LM. Adapting reflexes controlling the human posture. Exp Brain Res 26: 59–72, 1976.[ISI][Medline]

Owings TM, Pavol MJ, and Grabiner MD. Mechanisms of failed recovery following postural perturbations on a motorized treadmill mimic those associated with an actual forward trip. Clin Biomech 16: 813–819, 2001.[Medline]

Pai Y-C. Movement termination and stability in standing. Exerc Sport Sci Rev 31: 19–25, 2003.[ISI][Medline]

Pai Y-C and Iqbal K. Simulated movement termination for balance recovery: can movement strategies be sought to maintain stability even in the presence of slipping or forced sliding? J Biomech 32: 779–786, 1999.[ISI][Medline]

Pai Y-C, 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 Y-C and Patton JL. Center of mass velocity-position predictions for balance control. J Biomech 30: 347–354, 1997.[ISI][Medline]

Pai Y-C, 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 30: 1111–1118, 1998.

Patton JL, Pai Y, 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, Owings TM, and Grabiner MD. Body segment inertial parameter estimation for the general population of older adults. J Biomech 35: 707–712, 2002a.[ISI][Medline]

Pavol MJ and Pai Y-C. Feedforward adaptations are used to compensate for a potential loss of balance. Exp Brain Res 145: 528–538, 2002.[ISI][Medline]

Pavol MJ, Runtz EF, Edwards BJ, and Pai Y-C. Age influences the outcome of a slipping perturbation during initial but not repeated exposures. J Gerontol: Med Sci 57: M496–M503, 2002b.[Abstract/Free Full Text]

Pavol MJ, Runtz EF, and Pai Y-C. Diminished stepping responses lead to a fall following a novel slip induced during a sit-to-stand. Gait Posture In press.

Pavol MJ, Runtz EF, and Pai Y-C. Young and older adults exhibit proactive and reactive adaptations to repeated slip exposure. J Gerontol Med Sci In press.

Scheidt RA, Dingwell JB, and Mussa-Ivaldi FA. Learning to move amid uncertainty. J Neurophysiol 86: 971–985, 2001.[Abstract/Free Full Text]

Smeesters C, Hayes WC, and McMahon TA. Disturbance type and gait speed affect fall direction and impact location. J Biomech 34: 309–317, 2001.[ISI][Medline]

Stelmach GE and Worringham MA. Sensorimotor deficits related to postural stability: implications for falling in the elderly. Clin Geriat Med 1: 679–694, 1985.[Medline]

Tinetti ME, Speechley M, and Ginter SF. Risk factors for falls among elderly persons living in the community. N Engl J Med 319: 1701–1707, 1988.[Abstract]

Topper AK, Maki BE, and Holliday PJ. Are activity-based assessments of balance and gait in the elderly predictive of risk of falling and/or type of fall? J Am Geriat Soc 41: 479–487, 1993.[ISI][Medline]

Witney AG, Vetter P, and Wolpert DM. The influence of previous experience on predictive motor control. Neuroreport 12: 649–653, 2001.[ISI][Medline]

Wolpert DM and Ghahramani Z. Computational principles of movement neuroscience. Nat Neurosci 3: 1212–1217, 2000.

Wolpert DM, Ghahramani Z, and Jordan MI. An internal model for sensorimotor integration. Science 269: 1880–1882, 1995.[Abstract/Free Full Text]

Woollacott M, Tang P-F, and Lin S-I. Dynamic balance control in older adults: does limited response capacity lead to falls? In: From Basic Motor Control to Functional Recovery: Concepts, Theories and Models Present State and Perspective, edited by Gantchev N and Gantchev GN. Sofia, Bulgaria: Academic Publishing House "Prof. M. Drinov", 1999, p. 103–107.




This article has been cited by other articles:


Home page
J. Neurophysiol.Home page
K. L. Bunday and A. M. Bronstein
Visuo-vestibular Influences on the Moving Platform Locomotor Aftereffect
J Neurophysiol, March 1, 2008; 99(3): 1354 - 1365.
[Abstract] [Full Text] [PDF]


Home page
J. Neurophysiol.Home page
T. Bhatt and Y.-C. Pai
Can Observational Training Substitute Motor Training in Preventing Backward Balance Loss After an Unexpected Slip During Walking?
J Neurophysiol, February 1, 2008; 99(2): 843 - 852.
[Abstract] [Full Text] [PDF]


Home page
ptjournalHome page
Y.-C. Pai and T. S Bhatt
Repeated-Slip Training: An Emerging Paradigm for Prevention of Slip-Related Falls Among Older Adults
Physical Therapy, November 1, 2007; 87(11): 1478 - 1491.
[Abstract] [Full Text] [PDF]


Home page
J. Neurophysiol.Home page
T. Bhatt, E. Wang, and Y.-C. Pai
Retention of Adaptive Control Over Varying Intervals: Prevention of Slip- Induced Backward Balance Loss During Gait
J Neurophysiol, May 1, 2006; 95(5): 2913 - 2922.
[Abstract] [Full Text] [PDF]


Home page
J. Exp. Biol.Home page
K. Karamanidis and A. Arampatzis
Mechanical and morphological properties of different muscle-tendon units in the lower extremity and running mechanics: effect of aging and physical activity
J. Exp. Biol., October 15, 2005; 208(20): 3907 - 3923.
[Abstract] [Full Text] [PDF]


Home page
J. Neurophysiol.Home page
T. Bhatt and Y.-C. Pai
Long-Term Retention of Gait Stability Improvements
J Neurophysiol, September 1, 2005; 94(3): 1971 - 1979.
[Abstract] [Full Text] [PDF]


Home page
J. Gerontol. A Biol. Sci. Med. Sci.Home page
M. J. Pavol, E. F. Runtz, and Y.-C. Pai
Young and Older Adults Exhibit Proactive and Reactive Adaptations to Repeated Slip Exposure
J. Gerontol. A Biol. Sci. Med. Sci., May 1, 2004; 59(5): M494 - M502.
[Abstract] [Full Text] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend