Perceptual & Motor Skills: Motor Skills & Ergonomics 2013, 116, 3, 969-979. © Perceptual & Motor Skills 2013
POSTURAL CONTROL DURING PUSHING MOVEMENT WITH RISK OF FORWARD PERTURBATION1 RIKA OKAI
MOTOKO FUJIWARA
Graduate School of Human Culture Nara Women’s University, Japan
Human Behavior Science Nara Women’s University, Japan
Summary.—The purpose of this study was to investigate the effect of a forward bilateral pushing movement on postural control in a situation where known, unknown, and unpredictable perturbations may be induced. Participants stood upright and voluntarily pushed a handle with both hands. In the first task, the handle was free to be moved by the participant (perturbation; movable task) and in the second task, the handle was locked (stationary task). For each task, body displacement and observed applied force were recorded. Anticipatory postural control adjustment plays a vital role in body stability; however, in contrast to its role in maintaining stability, adjustment can generate a restricted voluntary movement because motor programming selects a postural control that gives priority to body stability over the target movement.
The ability to maintain body stability plays an important role in physical movement. The mechanism by which humans maintain stability in the upright standing position during voluntary movement has been examined in numerous studies of postural control. Anticipatory postural adjustments are triggered before voluntary movement to compensate for the upcoming perturbation induced by the voluntary movement. These anticipatory postural adjustments are typically some form of feed-forward control integrated into motor programming, and illustrate the ability to predict and compensate for self-generated perturbations (Kubiki, Bonnetblanc, Perement, Ballay, & Mourey, 2012). In this study, postural control was investigated in situations where multiple outcomes could be caused by an active movement. Segmental voluntary movements have been previously investigated, e.g., the joint movements of the shoulder (Horak, Esselman, Anderson, & Lynch, 1984; Bouisset & Zattara, 1987; Maki, 1993; Aruin & Latash, 1995; Vernazza, Cincera, Pedotti, & Massion, 1996) and elbow (Friedli, Hallet, & Simon, 1984; Friedli, Cohen, Hallet, Stanhope, & Simon, 1988), pushing and pulling a handle (Cordo & Nashner, 1982; Lee, Buchanan, & Rogers, 1987), and trunk bending (Oddsson & Thorstensson, 1986; Crenna, Frigo, Massion, & Pedotti, 1987; Pedotti, Crenna, Deat, Frigo, & Massion, 1989; Alexandrov, Alexander, & Massion, 1998). Segmental movements have also been examined in studies wherein the support base was transitory, Address correspondence to Rika Okai, Kitauoyanishi-machi, Nara, Japan or e-mail (car. [email protected]). 1
DOI 10.2466/26.22.PMS.116.3.969-979
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e.g., lower limb flexions or extensions (Rogers & Pai, 1990; Do, Nouillot, & Bouisset, 1991; Nouillot, Bouisset, & Do, 1992), and in studies featuring a transitory support base transfer, such as rising up on tiptoe (Lipshits, Mauritz, & Popov, 1981), rocking on heels (Nardone & Schieppati, 1988), and whole body reaching (Stapley, Pozzo, & Grishin, 1998; Tolambiya, Chiovetto, Pozzo, & Thomas, 2012) and lifting (Toussaint, Michies, Faber, Commissaris, & van Dieen, 1998; Commissaris, Toussaint, & Hirschfeld, 2001) tasks. Through a variety of experiments, it has been demonstrated that anticipatory postural adjustments contribute greatly to body stability while standing (Bouisset & Do, 2008). However, as a matter of course, the anticipation of necessary postural adjustments may not always be made under consistent conditions. This is especially true for situations requiring open skills, such as competitive sports; loss of balance is often observed when the movement of other players or other environmental features unexpectedly change. Loss of balance is an essential part of competitions such as judo, sumo wrestling, and rugby, in which the opponent’s movement may be predicted incorrectly or is unexpected. It has previously been reported that anticipatory postural adjustments can be observed even when the perturbation onset and velocity are unpredictably varied (Jacobs & Horak, 2007). Anticipatory postural adjustments are correlated with corrective responses (Toussaint, et al., 1998). To further investigate the mechanisms underlying postural control, the relationship between voluntary movement and postural control was examined in situations where the perturbation may be caused by the result of moving an object, in addition to a voluntary movement. In this study, participants were asked to push a handle with both hands. The handles could be moved in the forward direction under three conditions, with different predictability of the handle movement. Predictability was manipulated by changing the instruction given to the participants. Based on the findings of numerous studies of anticipatory postural adjustment, it was expected that the predictability of the perturbation would contribute to body stability during the perturbation when performing a voluntary movement. The goal of this study was to examine participants’ anticipatory postural adjustments when the predictability of a perturbation was manipulated. METHOD Participants Eight healthy, young-adult women were recruited from intact Nara Women’s university sports science classes (M age = 20.9 yr., SD = 1.2; M height = 154.0 cm, SD = 15.3; M weight = 102.5 lb., SD = 21.2) volunteered
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to participate in this study. None of the participants reported any neurological or neuromuscular disorders. The experiment conformed to the ethical principles outlined in the Declaration of Helsinki. Prior to experiment onset, informed consent was obtained from all participants according to the protocol of the local ethics committee. Apparatus Pushing force was measured by using a device (Takei Scientific Instruments Co., Ltd., Osaka, Japan) with two handles that could be locked or unlocked (Fig. 1). The handle was mounted on a track and could slide forward by 35 cm with low, variable, experimenter-controlled friction when the brake was unlocked. Pushing the handle in the unlocked position caused the participant to fall forward with no friction, i.e., elicited a large perturbation in the forward direction. The remotely controlled brake was not visible to the participants, and thus the “locked” and “unlocked” positions were not apparent. The handle was set at chest height for each participant. The distance between the two handles (right and left) was 40 cm. A black circle (2.0 cm in diameter) was placed as a gaze point approximately 70 cm in front of the participants at eye level.
FIG. 1. Illustration of the experimental setup showing the start position and the tasks, as viewed from the subject’s sagittal plane. The participant is pushing the handle toward the left. Pushing the lever in the unlocked position causes the participant to fall in the Perturbation task. The lever was locked in the Stationary task.
Movement, Tasks, and Conditions Each participant stood in an upright position with their feet parallel at shoulder-width and gripped the handles with both hands (Fig. 1). In the starting position, the participant was asked to gaze at the black circle and grip the handle with a 120º flexion of the elbow joint. The horizon distance between the top of the participant’s toe and the vertical axis of the handle was 25.4 cm (SD = 3.3). The participant was asked to push the handle as forcefully and as quickly as possible when the auditory signal was given.
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There were two tasks: (1) the unlocked handle moved easily in the forward direction (Perturbation task); (2) the locked handle did not move at all (Stationary task). In the Perturbation task, the applied force at which movement of the handle was triggered was set to a random value between 10% and 40% of the maximal pushing strength of each participant. Trigger forces were chosen to be small enough that participants would not be injured if they fell forward, but large enough that an effort was required to push the handle. Three conditions enabled investigation of the effect of predictability on perturbation. In the Known condition, the participant was informed that the handle would move when pushed. In the Unknown condition, the participant was not informed that the handle would move. Finally, in the Unpredictable condition, the participant was informed that the handle would not move. Under the Known and Unknown conditions, in order to obtain sufficient data reasonably, 24 trials were carried out in a randomized order, comprising 12 trials with the Perturbation task and 12 with the Stationary task. Under the Unpredictable condition, the Perturbation task was conducted only once, following 11 trials of the Stationary task (analysis trial, n = 1). The experimental conditions were administered in the following order: Known, Unknown, and Unpredictable. To reduce participant fatigue, a rest interval of 5 min. was provided between each condition. Each trial started with an auditory beep (500 Hz); a warning signal and a start signal were subsequently presented after a random interval between 2,000 and 4,000 msec. Under each condition and task, the participants were instructed to push the handle forcefully and quickly at full strength, applying even force with both hands. They were also asked to regain their standing posture if the handle moved (in the Known and Unknown conditions). Maximal pushing strength was measured using a common device. The participants practiced the handle push movement at 30% maximum force, performing 8 trials before the experiment. Data Acquisition and Analysis A camera (Sony CCD–F330) placed 3 m from the participant’s sagittal axis recorded the movement of seven markers (15 mm in diameter) placed at different anatomical sites on the participant. The sampling frequency was 60 Hz. Markers were placed on the participant’s left side at the following sites: the head (the auditory meatus of the ear), the upper limb (acromial process of the shoulder, lateral condyle of the elbow, and styloid process of the wrist), and the lower limb (the greater trochanter, knee interstitial joint space, and ankle external malleolus). The movement analysis system (DIPP–Motions 2D; Direct Co., Ltd., Japan, Tokyo) recorded and reconstructed successive images (every 16.6
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msec.). Body position displacement of the head, shoulder, hip, and knee were calculated in the anterior-posterior direction. Bilateral pushing strength data were recorded separately (right and left hands) with a strain gauge set up in the handle; this was digitized at 1,000 Hz for approximately 3,000 msec. by using an MP150 data acquisition system (Biopac Systems, Goleta, CA) and then passed through a digital filter with a 10-Hz low-pass cutoff. In order to evaluate pushing strength, we measured the integral of applied force from the time that the pushing force changed from a negative value to a positive value (t0), to the time that maximum applied force was reached (as measured for each participant in the stationary task). The data for right-hand pushing force was used to trigger the handle movement in the movable task, while the data for left-hand pushing force was used in the experimental analysis. With the acquired data, the effect of handle movement predictability on forward perturbation of the body during the pushing movement was evaluated for each task. Student’s t test was used to analyze the stationary task within participants. One-way analysis of variance (ANOVA) was used to assess the Perturbation task. When ANOVA indicated a statistically significant effect (p < .05), pairwise comparisons were carried out between conditions using Bonferroni adjustment. RESULTS General Characteristics of Movements Figure 2 presents the movement data of one participant in the Unpredictable trial and their mean movements (7 trials) under the Known and Unknown conditions. A bold line shows a starting position and the postural changes that occurred while pushing, per 100 msec. In the Unpredictable trial, all participants took forward compensatory steps to recover balance in response to forward translations of the handle. Balance was lost completely by all participants; the position of the head, shoulder, hip, and knee shifted suddenly in the forward direction (Fig. 2A). In the Perturbation task under the Known and Unknown conditions, participants pushed the handle without forward compensatory steps to recover balance. Under both of these conditions, each participant exhibited similar whole-body movement characteristics (Fig. 2A). In the Stationary task, the position of each body part shifted forward under the Known condition but not under the Unknown condition. Under the Unknown condition, a backward hip displacement was observed following movement onset (Fig. 2B). Table 1 shows the mean forward displacement (all 8 participants) of the head, shoulder, hip, and knee markers for each task under all conditions. Forward displacements were markedly less in the Perturbation task under the Known and Unknown conditions than under the Unpredictable
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FIG. 2. General characteristics of whole-body pushing movement for one participant. Seven trials averaged in the sagittal plane for movements executed under the Known and Unknown conditions, and one trial of the Perturbation task under the Unpredictable condition. A and B show the movement in the Perturbation and Stationary tasks, respectively. The bold line shows posture at the start position.
trial for the head (η2 = 0.68), shoulder (η2 = 0.71), hip (η2 = 0.87), and knee (η2 = 0.89). No statistically significant difference was found between forward displacements under the Known and Unknown conditions for each body part. In the Stationary task, the displacement of each body part was less under the Unknown condition than the Known condition for the head (Cohen’s d = 0.65), shoulder (d = 0.71), hip (d = 0.88), and knee (d = 0.87). In particular, a notable decrease was observed for the hip and knee under the Unknown condition. Pushing Strength in the Stationary Task Before and after the experiment, maximal pushing force was measured for each participant. It was confirmed that no statistically significant difference existed in these values (t7 = 1.04, p > .33), and thus, fatigue had no influence on the results of the experiment. Fig. 3A shows a typical example of unilateral (left hand) pushing force in the stationary task under the Known and Unknown conditions. The integral of the pushing force from t0 to the maximum applied force was less (t7 = 4.13, p < .01, Cohen’s d = 0.71) and maximum pushing force was applied earlier (t7 = 2.96, p < .05, Cohen’s d = 0.67) under the Unknown
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TABLE 1 DESCRIPTIVE STATISTICS FOR FORWARD DISPLACEMENT OF HEAD, SHOULDER, HIP, AND KNEE FOR ALL PARTICIPANTS IN (A) PERTURBATION AND (B) STATIONARY TASKS A
Unpredictable
Known
M
SD
M
SD
Unknown M
SD
df
F
Post hoc Comparison UP > K†, UK†
Head
59.9
15.2
32.30
15.4
41.9 14.8
2,21
11.02
Shoulder
51.4
15.5
22.80
11.4
34.2 11.0
2,21
13.05
UP > K‡, UK†
Hip
33.3
13.3
10.50
4.7
14.9
6.0
2,21
23.32
UP > K‡, UK‡
Knee
28.6
15.1
5.72
2.0
8.6
3.4
2,21
87.42
UP > K‡, UK‡
B
Known
Unknown
df
t
9.8
7
2.49
K < UK*
8.3
7
4.30
K < UK†
5.4
7
10.34
K < UK‡
M
SD
M
SD
Head
31.4
9.5
28.3
Shoulder
23.8
5.7
18.0
Hip
19.0
4.2
7.6
Post hoc Comparison
Knee 9.5 3.4 3.9 1.9 7 10.28 K < UK‡ Note.—UP = Unpredictable; K = Known; UK = Unknown. There were no significant differences between the K, UK conditions at all. *p < .05. †p < .01. ‡p < .001.
condition than under the Known condition (Fig. 3B). The maximum value of the pushing force showed no statistically significant difference between the conditions (t7 = 0.03, p > .97). DISCUSSION The results clearly indicated that the postural responses to the handle movement under the Known and Unknown conditions were different from that of the Unpredictable condition. Although participants experienced 24 trials of the Perturbation task prior to the Unpredictable trial, they were not successful in maintaining their body stability when unable to predict the movement of the handle. This result suggests that equilibrium of the body cannot be maintained simply by using prior experience and online compensatory processes, when the postural perturbation was too large and too fast. The results show that stability when the handle moved depended on the feed-forward system based on the predictability of the handle’s movement. Under the Known and Unknown conditions, movement of the body in the forward direction was small and body stability was completely maintained. In comparison with the Unpredictable trial, the relative forward displacements of the hip and the knee were 35.2% (SD = 14.5) and 21.3% (SD = 11.8), respectively, of that under the Known condition, and 34.2% (SD = 18.3) and 21.6% (SD = 9.6), respectively, of that under the Unknown condition. A similar strategy for preventing excessive forward bend was
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A 100
max Known Unknown
N
60 20
–20 –60
t0
1s Duration
††
*
10 5 0
200 100 0
Max 150 Force (N)
Work (Nm)
15
Integral Duration (msec.)
B
Known Unknown
100 50 0
FIG. 3. Pushing force in the Stationary task. A. A typical example of pushing strength across seven trials for one participant. B. Mean and standard deviation of integral, duration, and maximum applied force (i.e., shaded area of curvilinear pushing strength) for all participants under the Known and Unknown conditions. Statistically significant differences between conditions *p < .05, †p < .01.
employed by all participants, showing anticipatory postural control based on the predicted perturbation, as observed in previous studies (Bouisset & Do, 2008). Although individual differences were observed in the movement of each participant’s body parts under both the Known and Unknown conditions, these differences were small and the observed characteristics of the changes in posture were similar. This observation suggests that the effects of differing predictability were small when participants were aware of the possibility that the handle would move prior to the pushing movement. Postural control was maintained even when the predictability of the perturbation varied in the Perturbation task. In contrast to the Perturbation task, movement in the Stationary task was notably different under the Known and Unknown conditions. Under Unknown conditions, all participants exhibited a statistically significant decrease in the forward displacement of the body; displacements of the head, shoulder, hip, and knee were 78.5% (SD = 34.8), 63.5% (SD = 28.1),
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35.6% (SD = 19.3), and 43.4% (SD = 13.7), respectively, of that under the Known condition. The time course of the changing position of the body was similar for the head and shoulder, but large individual variations were observed for the hip and knee. These results demonstrate that the postural stability strategy emphasizes changes in the position of the hip and knee. Based on the comparisons between the Known and Unknown conditions for each task, it appears that the effects of handle-movement predictability on postural changes were larger in the stationary task than the movable task. This suggests that the pushing movement was accomplished based on a postural control strategy that more strongly considered the possibility of handle movement, perhaps because of the relatively higher danger of stability loss in that case. A postural control strategy based on the predictability of the perturbation greatly contributed to body stability when it occurred. Regardless of the handle-movement predictability, postural control strategy seems to be based on the situation with higher risk of perturbation. Therefore, the required movement under uncertain predictability may be greatly constrained by anticipated postural control adjustments, which play a vital role in body stability. Anticipated postural control adjustment could generate restricted dynamic movements in competitive sports, since motor programming selects a postural control strategy prioritizing body stability over the required movement. In recent research, it has been demonstrated that the central nervous system is capable of implementing multiple strategies while controlling the position of the body in space. Jacobs and Horak (2007) showed that even when the direction and speed of the postural perturbation was unpredictable and the postural responses had to be selected and initiated before being influenced by online visuomotor processes, participants preselected their stepping limb to comply with potential environmental constraints to reach a potential target while still maintaining stability. In this study, there was no tendency for a postural control strategy based on both experimental tasks, even though the tasks were designed like Jacobs and Horak’s; the results clearly show that a postural control strategy was preselected before feedback information was received when two or more outcomes could be caused by the pushing movement. The main finding of the present study is that motor programming selects a postural control strategy that prioritizes body stability. Future studies should not only investigate the benefits of anticipated postural adjustment, but also the negative effects on movement. This information will help understand postural control in a situation where posture is continuously and largely changing and the predictability of perturbations is uncertain, such as in sports competitions.
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ALEXANDROV, A., ALEXANDER, F., & MASSION, J. (1998) Axial synergies during human upper trunk bending. Experimental Brain Research, 118, 210-220. ARUIN, A. S., & LATASH, M. L. (1995) Directional specificity of postural muscles in feedforward postural reactions during fast voluntary arm movements. Experimental Brain Research, 103, 323-332. BOUISSET, S., & DO, M. C. (2008) Posture, dynamic stability, and voluntary movement. Neurophysiologie Clinique, 38, 345-362. BOUISSET, S., & ZATTARA, M. (1987) Biomechanical study of the programming of anticipatory postural adjustments associated with voluntary movement. Journal of Biomechanics, 20, 735-742. COMMISSARIS, D. A. C. M., TOUSSAINT, H. M., & HIRSCHFELD, H. (2001) Anticipatory postural adjustments in a bimanual, whole-body lifting task seem not only aimed at minimizing anterior-posterior center of mass. Gait & Posture, 14, 44-55. CORDO, P. J., & NASHNER, L. M. (1982) Properties of postural movements related to a voluntary movement. Journal of Neurophysiology, 47, 287-303. CRENNA, P., FRIGO, C., MASSION, J., & PEDOTTI, A. (1987) Forward and backward axial synergies in man. Experimental Brain Research, 65, 538-548. DO, M. C., NOUILLOT, P. H., & BOUISSET, S. (1991) Is balance or posture at the end of a voluntary movement programmed? Neuroscience Letters, 130, 9-11. FRIEDLI, W. G., COHEN, L., HALLETT, M., STANHOPE, S., & SIMON, S. R. (1988) Postural adjustments associated with rapid arm movements: biomechanical analysis. Journal of Neurology, Neurosurgery, and Psychiatry, 51, 232-243. FRIEDLI, W. G., HALLETT, M., & SIMON, S. R. (1984) Postural adjustments associated with rapid arm movements 1. Electromyographic data. Journal of Neurology, Neurosurgery, and Psychiatry, 47, 611-622. JACOBS, J. V., & HORAK, F. B. (2007) External postural perturbations induce multiple anticipatory postural adjustments when participants cannot pre-select their stepping foot. Experimental Brain Research, 179, 29-42. HORAK, F. B., ESSELMAN, P. E., ANDERSON, M. E., & LYNCH, M. K. (1984) The effect of movement velocity, mass displaced and task certainty on associated postural adjustments made by normal and hemiplegic individuals. Journal of Neurology, Neurosurgery, and Psychiatry, 47, 1020-1028. KUBIKI, A., BONNETBLANC, F., PEREMENT, G., BALLAY, Y., & MOUREY, F. (2012) Delayed postural control self-generated perturbation in the frail order adults. Clinical Interventions in Aging, 7, 65-75. LEE, W. A., BUCHANAN, T. S., & ROGERS, M. W. (1987) Effects of arm acceleration and behavioral conditions on the organization of postural adjustments during arm flexion. Experimental Brain Research, 66, 257-270. LIPSHITS, M., MAURITZ, K., & POPOV, K. E. (1981) Quantitative analysis of anticipatory postural components of a complex voluntary movement. Human Physiology, 7, 165-173. MAKI, B. E. (1993) Biomechanical approach to quantifying anticipatory postural adjustments in the elderly. Medical and Biological Engineering and Computing, 31, 355-362. NARDONE, A., & SCHIEPPATI, M. (1988) Postural adjustments associated with voluntary contractions of leg muscles in standing man. Experimental Brain Research, 69, 469480.
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NOUILLOT, P., BOUISSET, S., & DO, M. C. (1992) Do fast voluntary movements necessitate anticipatory postural adjustments even if equilibrium unstable? Neuroscience Letters, 147, 1-4. ODDSSON, L., & THORSTENSSON, A. (1986) Fast voluntary trunk flexion movements in standing: primary movements and associated postural adjustments. Acta Physiologica Scandinavica, 128, 341-349. PEDOTTI, A., CRENNA, P., DEAT, A., FRIGO, C., & MASSION J. (1989) Postural synergies in axial movements: short and long-term adaptation. Experimental Brain Research, 74, 3-10. ROGERS, M. W., & PAI, Y. C. (1990) Dynamic transitions in stance support accompanying leg flexion movements in man. Experimental Brain Research, 81, 398-402. STAPLEY, P., POZZO, T., & GRISHIN, A. (1998) The role of anticipatory postural adjustments during whole body reaching movements. NeuroReport, 9, 395-401. TOLAMBIYA, A., CHIOVETTO, E., POZZO, T., & THOMAS, E. (2012) Modulation of anticipatory postural activity for multiple conditions of whole-body pointing task. Neuroscience, 210, 179-190. TOUSSAINT, H. M., MICHIES, Y. M., FABER, M. N., COMMISSARIS, D. A. C. M., & VAN DIEEN, J. H. (1998) Scaling anticipatory postural adjustments dependent on confidence of load estimation in a bimanual whole-body lifting task. Experimental Brain Research, 120, 85-94. VERNAZZA, S., CINCERA, M., PEDOTTI, A., & MASSION, J. (1996) Balance control during lateral arm raising in humans. NeuroReport, 7, 1543-1548. Accepted May 31, 2013.
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POSTURAL CONTROL DURING PUSHING MOVEMENT WITH RISK OF FORWARD PERTURBATION1 RIKA OKAI
MOTOKO FUJIWARA
Graduate School of Human Culture Nara Women’s University, Japan
Human Behavior Science Nara Women’s University, Japan
Summary.—The purpose of this study was to investigate the effect of a forward bilateral pushing movement on postural control in a situation where known, unknown, and unpredictable perturbations may be induced. Participants stood upright and voluntarily pushed a handle with both hands. In the first task, the handle was free to be moved by the participant (perturbation; movable task) and in the second task, the handle was locked (stationary task). For each task, body displacement and observed applied force were recorded. Anticipatory postural control adjustment plays a vital role in body stability; however, in contrast to its role in maintaining stability, adjustment can generate a restricted voluntary movement because motor programming selects a postural control that gives priority to body stability over the target movement.
The ability to maintain body stability plays an important role in physical movement. The mechanism by which humans maintain stability in the upright standing position during voluntary movement has been examined in numerous studies of postural control. Anticipatory postural adjustments are triggered before voluntary movement to compensate for the upcoming perturbation induced by the voluntary movement. These anticipatory postural adjustments are typically some form of feed-forward control integrated into motor programming, and illustrate the ability to predict and compensate for self-generated perturbations (Kubiki, Bonnetblanc, Perement, Ballay, & Mourey, 2012). In this study, postural control was investigated in situations where multiple outcomes could be caused by an active movement. Segmental voluntary movements have been previously investigated, e.g., the joint movements of the shoulder (Horak, Esselman, Anderson, & Lynch, 1984; Bouisset & Zattara, 1987; Maki, 1993; Aruin & Latash, 1995; Vernazza, Cincera, Pedotti, & Massion, 1996) and elbow (Friedli, Hallet, & Simon, 1984; Friedli, Cohen, Hallet, Stanhope, & Simon, 1988), pushing and pulling a handle (Cordo & Nashner, 1982; Lee, Buchanan, & Rogers, 1987), and trunk bending (Oddsson & Thorstensson, 1986; Crenna, Frigo, Massion, & Pedotti, 1987; Pedotti, Crenna, Deat, Frigo, & Massion, 1989; Alexandrov, Alexander, & Massion, 1998). Segmental movements have also been examined in studies wherein the support base was transitory, Address correspondence to Rika Okai, Kitauoyanishi-machi, Nara, Japan or e-mail (car. [email protected]). 1
DOI 10.2466/26.22.PMS.116.3.969-979
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e.g., lower limb flexions or extensions (Rogers & Pai, 1990; Do, Nouillot, & Bouisset, 1991; Nouillot, Bouisset, & Do, 1992), and in studies featuring a transitory support base transfer, such as rising up on tiptoe (Lipshits, Mauritz, & Popov, 1981), rocking on heels (Nardone & Schieppati, 1988), and whole body reaching (Stapley, Pozzo, & Grishin, 1998; Tolambiya, Chiovetto, Pozzo, & Thomas, 2012) and lifting (Toussaint, Michies, Faber, Commissaris, & van Dieen, 1998; Commissaris, Toussaint, & Hirschfeld, 2001) tasks. Through a variety of experiments, it has been demonstrated that anticipatory postural adjustments contribute greatly to body stability while standing (Bouisset & Do, 2008). However, as a matter of course, the anticipation of necessary postural adjustments may not always be made under consistent conditions. This is especially true for situations requiring open skills, such as competitive sports; loss of balance is often observed when the movement of other players or other environmental features unexpectedly change. Loss of balance is an essential part of competitions such as judo, sumo wrestling, and rugby, in which the opponent’s movement may be predicted incorrectly or is unexpected. It has previously been reported that anticipatory postural adjustments can be observed even when the perturbation onset and velocity are unpredictably varied (Jacobs & Horak, 2007). Anticipatory postural adjustments are correlated with corrective responses (Toussaint, et al., 1998). To further investigate the mechanisms underlying postural control, the relationship between voluntary movement and postural control was examined in situations where the perturbation may be caused by the result of moving an object, in addition to a voluntary movement. In this study, participants were asked to push a handle with both hands. The handles could be moved in the forward direction under three conditions, with different predictability of the handle movement. Predictability was manipulated by changing the instruction given to the participants. Based on the findings of numerous studies of anticipatory postural adjustment, it was expected that the predictability of the perturbation would contribute to body stability during the perturbation when performing a voluntary movement. The goal of this study was to examine participants’ anticipatory postural adjustments when the predictability of a perturbation was manipulated. METHOD Participants Eight healthy, young-adult women were recruited from intact Nara Women’s university sports science classes (M age = 20.9 yr., SD = 1.2; M height = 154.0 cm, SD = 15.3; M weight = 102.5 lb., SD = 21.2) volunteered
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to participate in this study. None of the participants reported any neurological or neuromuscular disorders. The experiment conformed to the ethical principles outlined in the Declaration of Helsinki. Prior to experiment onset, informed consent was obtained from all participants according to the protocol of the local ethics committee. Apparatus Pushing force was measured by using a device (Takei Scientific Instruments Co., Ltd., Osaka, Japan) with two handles that could be locked or unlocked (Fig. 1). The handle was mounted on a track and could slide forward by 35 cm with low, variable, experimenter-controlled friction when the brake was unlocked. Pushing the handle in the unlocked position caused the participant to fall forward with no friction, i.e., elicited a large perturbation in the forward direction. The remotely controlled brake was not visible to the participants, and thus the “locked” and “unlocked” positions were not apparent. The handle was set at chest height for each participant. The distance between the two handles (right and left) was 40 cm. A black circle (2.0 cm in diameter) was placed as a gaze point approximately 70 cm in front of the participants at eye level.
FIG. 1. Illustration of the experimental setup showing the start position and the tasks, as viewed from the subject’s sagittal plane. The participant is pushing the handle toward the left. Pushing the lever in the unlocked position causes the participant to fall in the Perturbation task. The lever was locked in the Stationary task.
Movement, Tasks, and Conditions Each participant stood in an upright position with their feet parallel at shoulder-width and gripped the handles with both hands (Fig. 1). In the starting position, the participant was asked to gaze at the black circle and grip the handle with a 120º flexion of the elbow joint. The horizon distance between the top of the participant’s toe and the vertical axis of the handle was 25.4 cm (SD = 3.3). The participant was asked to push the handle as forcefully and as quickly as possible when the auditory signal was given.
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There were two tasks: (1) the unlocked handle moved easily in the forward direction (Perturbation task); (2) the locked handle did not move at all (Stationary task). In the Perturbation task, the applied force at which movement of the handle was triggered was set to a random value between 10% and 40% of the maximal pushing strength of each participant. Trigger forces were chosen to be small enough that participants would not be injured if they fell forward, but large enough that an effort was required to push the handle. Three conditions enabled investigation of the effect of predictability on perturbation. In the Known condition, the participant was informed that the handle would move when pushed. In the Unknown condition, the participant was not informed that the handle would move. Finally, in the Unpredictable condition, the participant was informed that the handle would not move. Under the Known and Unknown conditions, in order to obtain sufficient data reasonably, 24 trials were carried out in a randomized order, comprising 12 trials with the Perturbation task and 12 with the Stationary task. Under the Unpredictable condition, the Perturbation task was conducted only once, following 11 trials of the Stationary task (analysis trial, n = 1). The experimental conditions were administered in the following order: Known, Unknown, and Unpredictable. To reduce participant fatigue, a rest interval of 5 min. was provided between each condition. Each trial started with an auditory beep (500 Hz); a warning signal and a start signal were subsequently presented after a random interval between 2,000 and 4,000 msec. Under each condition and task, the participants were instructed to push the handle forcefully and quickly at full strength, applying even force with both hands. They were also asked to regain their standing posture if the handle moved (in the Known and Unknown conditions). Maximal pushing strength was measured using a common device. The participants practiced the handle push movement at 30% maximum force, performing 8 trials before the experiment. Data Acquisition and Analysis A camera (Sony CCD–F330) placed 3 m from the participant’s sagittal axis recorded the movement of seven markers (15 mm in diameter) placed at different anatomical sites on the participant. The sampling frequency was 60 Hz. Markers were placed on the participant’s left side at the following sites: the head (the auditory meatus of the ear), the upper limb (acromial process of the shoulder, lateral condyle of the elbow, and styloid process of the wrist), and the lower limb (the greater trochanter, knee interstitial joint space, and ankle external malleolus). The movement analysis system (DIPP–Motions 2D; Direct Co., Ltd., Japan, Tokyo) recorded and reconstructed successive images (every 16.6
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msec.). Body position displacement of the head, shoulder, hip, and knee were calculated in the anterior-posterior direction. Bilateral pushing strength data were recorded separately (right and left hands) with a strain gauge set up in the handle; this was digitized at 1,000 Hz for approximately 3,000 msec. by using an MP150 data acquisition system (Biopac Systems, Goleta, CA) and then passed through a digital filter with a 10-Hz low-pass cutoff. In order to evaluate pushing strength, we measured the integral of applied force from the time that the pushing force changed from a negative value to a positive value (t0), to the time that maximum applied force was reached (as measured for each participant in the stationary task). The data for right-hand pushing force was used to trigger the handle movement in the movable task, while the data for left-hand pushing force was used in the experimental analysis. With the acquired data, the effect of handle movement predictability on forward perturbation of the body during the pushing movement was evaluated for each task. Student’s t test was used to analyze the stationary task within participants. One-way analysis of variance (ANOVA) was used to assess the Perturbation task. When ANOVA indicated a statistically significant effect (p < .05), pairwise comparisons were carried out between conditions using Bonferroni adjustment. RESULTS General Characteristics of Movements Figure 2 presents the movement data of one participant in the Unpredictable trial and their mean movements (7 trials) under the Known and Unknown conditions. A bold line shows a starting position and the postural changes that occurred while pushing, per 100 msec. In the Unpredictable trial, all participants took forward compensatory steps to recover balance in response to forward translations of the handle. Balance was lost completely by all participants; the position of the head, shoulder, hip, and knee shifted suddenly in the forward direction (Fig. 2A). In the Perturbation task under the Known and Unknown conditions, participants pushed the handle without forward compensatory steps to recover balance. Under both of these conditions, each participant exhibited similar whole-body movement characteristics (Fig. 2A). In the Stationary task, the position of each body part shifted forward under the Known condition but not under the Unknown condition. Under the Unknown condition, a backward hip displacement was observed following movement onset (Fig. 2B). Table 1 shows the mean forward displacement (all 8 participants) of the head, shoulder, hip, and knee markers for each task under all conditions. Forward displacements were markedly less in the Perturbation task under the Known and Unknown conditions than under the Unpredictable
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FIG. 2. General characteristics of whole-body pushing movement for one participant. Seven trials averaged in the sagittal plane for movements executed under the Known and Unknown conditions, and one trial of the Perturbation task under the Unpredictable condition. A and B show the movement in the Perturbation and Stationary tasks, respectively. The bold line shows posture at the start position.
trial for the head (η2 = 0.68), shoulder (η2 = 0.71), hip (η2 = 0.87), and knee (η2 = 0.89). No statistically significant difference was found between forward displacements under the Known and Unknown conditions for each body part. In the Stationary task, the displacement of each body part was less under the Unknown condition than the Known condition for the head (Cohen’s d = 0.65), shoulder (d = 0.71), hip (d = 0.88), and knee (d = 0.87). In particular, a notable decrease was observed for the hip and knee under the Unknown condition. Pushing Strength in the Stationary Task Before and after the experiment, maximal pushing force was measured for each participant. It was confirmed that no statistically significant difference existed in these values (t7 = 1.04, p > .33), and thus, fatigue had no influence on the results of the experiment. Fig. 3A shows a typical example of unilateral (left hand) pushing force in the stationary task under the Known and Unknown conditions. The integral of the pushing force from t0 to the maximum applied force was less (t7 = 4.13, p < .01, Cohen’s d = 0.71) and maximum pushing force was applied earlier (t7 = 2.96, p < .05, Cohen’s d = 0.67) under the Unknown
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TABLE 1 DESCRIPTIVE STATISTICS FOR FORWARD DISPLACEMENT OF HEAD, SHOULDER, HIP, AND KNEE FOR ALL PARTICIPANTS IN (A) PERTURBATION AND (B) STATIONARY TASKS A
Unpredictable
Known
M
SD
M
SD
Unknown M
SD
df
F
Post hoc Comparison UP > K†, UK†
Head
59.9
15.2
32.30
15.4
41.9 14.8
2,21
11.02
Shoulder
51.4
15.5
22.80
11.4
34.2 11.0
2,21
13.05
UP > K‡, UK†
Hip
33.3
13.3
10.50
4.7
14.9
6.0
2,21
23.32
UP > K‡, UK‡
Knee
28.6
15.1
5.72
2.0
8.6
3.4
2,21
87.42
UP > K‡, UK‡
B
Known
Unknown
df
t
9.8
7
2.49
K < UK*
8.3
7
4.30
K < UK†
5.4
7
10.34
K < UK‡
M
SD
M
SD
Head
31.4
9.5
28.3
Shoulder
23.8
5.7
18.0
Hip
19.0
4.2
7.6
Post hoc Comparison
Knee 9.5 3.4 3.9 1.9 7 10.28 K < UK‡ Note.—UP = Unpredictable; K = Known; UK = Unknown. There were no significant differences between the K, UK conditions at all. *p < .05. †p < .01. ‡p < .001.
condition than under the Known condition (Fig. 3B). The maximum value of the pushing force showed no statistically significant difference between the conditions (t7 = 0.03, p > .97). DISCUSSION The results clearly indicated that the postural responses to the handle movement under the Known and Unknown conditions were different from that of the Unpredictable condition. Although participants experienced 24 trials of the Perturbation task prior to the Unpredictable trial, they were not successful in maintaining their body stability when unable to predict the movement of the handle. This result suggests that equilibrium of the body cannot be maintained simply by using prior experience and online compensatory processes, when the postural perturbation was too large and too fast. The results show that stability when the handle moved depended on the feed-forward system based on the predictability of the handle’s movement. Under the Known and Unknown conditions, movement of the body in the forward direction was small and body stability was completely maintained. In comparison with the Unpredictable trial, the relative forward displacements of the hip and the knee were 35.2% (SD = 14.5) and 21.3% (SD = 11.8), respectively, of that under the Known condition, and 34.2% (SD = 18.3) and 21.6% (SD = 9.6), respectively, of that under the Unknown condition. A similar strategy for preventing excessive forward bend was
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A 100
max Known Unknown
N
60 20
–20 –60
t0
1s Duration
††
*
10 5 0
200 100 0
Max 150 Force (N)
Work (Nm)
15
Integral Duration (msec.)
B
Known Unknown
100 50 0
FIG. 3. Pushing force in the Stationary task. A. A typical example of pushing strength across seven trials for one participant. B. Mean and standard deviation of integral, duration, and maximum applied force (i.e., shaded area of curvilinear pushing strength) for all participants under the Known and Unknown conditions. Statistically significant differences between conditions *p < .05, †p < .01.
employed by all participants, showing anticipatory postural control based on the predicted perturbation, as observed in previous studies (Bouisset & Do, 2008). Although individual differences were observed in the movement of each participant’s body parts under both the Known and Unknown conditions, these differences were small and the observed characteristics of the changes in posture were similar. This observation suggests that the effects of differing predictability were small when participants were aware of the possibility that the handle would move prior to the pushing movement. Postural control was maintained even when the predictability of the perturbation varied in the Perturbation task. In contrast to the Perturbation task, movement in the Stationary task was notably different under the Known and Unknown conditions. Under Unknown conditions, all participants exhibited a statistically significant decrease in the forward displacement of the body; displacements of the head, shoulder, hip, and knee were 78.5% (SD = 34.8), 63.5% (SD = 28.1),
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35.6% (SD = 19.3), and 43.4% (SD = 13.7), respectively, of that under the Known condition. The time course of the changing position of the body was similar for the head and shoulder, but large individual variations were observed for the hip and knee. These results demonstrate that the postural stability strategy emphasizes changes in the position of the hip and knee. Based on the comparisons between the Known and Unknown conditions for each task, it appears that the effects of handle-movement predictability on postural changes were larger in the stationary task than the movable task. This suggests that the pushing movement was accomplished based on a postural control strategy that more strongly considered the possibility of handle movement, perhaps because of the relatively higher danger of stability loss in that case. A postural control strategy based on the predictability of the perturbation greatly contributed to body stability when it occurred. Regardless of the handle-movement predictability, postural control strategy seems to be based on the situation with higher risk of perturbation. Therefore, the required movement under uncertain predictability may be greatly constrained by anticipated postural control adjustments, which play a vital role in body stability. Anticipated postural control adjustment could generate restricted dynamic movements in competitive sports, since motor programming selects a postural control strategy prioritizing body stability over the required movement. In recent research, it has been demonstrated that the central nervous system is capable of implementing multiple strategies while controlling the position of the body in space. Jacobs and Horak (2007) showed that even when the direction and speed of the postural perturbation was unpredictable and the postural responses had to be selected and initiated before being influenced by online visuomotor processes, participants preselected their stepping limb to comply with potential environmental constraints to reach a potential target while still maintaining stability. In this study, there was no tendency for a postural control strategy based on both experimental tasks, even though the tasks were designed like Jacobs and Horak’s; the results clearly show that a postural control strategy was preselected before feedback information was received when two or more outcomes could be caused by the pushing movement. The main finding of the present study is that motor programming selects a postural control strategy that prioritizes body stability. Future studies should not only investigate the benefits of anticipated postural adjustment, but also the negative effects on movement. This information will help understand postural control in a situation where posture is continuously and largely changing and the predictability of perturbations is uncertain, such as in sports competitions.
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R. OKAI & M. FUJIWARA REFERENCES
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