Exp Brain Res DOI 10.1007/s00221-007-0932-1 R ES EA R C H A R TI CLE Prospective dynamic balance control in healthy children and adults Hanne Austad · Audrey L. H. van der Meer Received: 26 June 2006 / Accepted: 27 February 2007 © Springer-Verlag 2007 Abstract Balance control during gait initiation was studied using center of pressure (CoP) data from force plate measurements. Twenty-four participants were divided into four age groups: (1) 2–3 years, (2) 4–5 years, (3) 7–8 years, and (4) adults. Movement in the antero-posterior (CoPy) direction during the initial step was tau-G analyzed, investigating the hypothesis that tau of the CoPy motion-gap (CoPy), i.e., the time it will take to close the gap at its current closure rate, is tau-coupled onto an intrinsic tau-G guide (G), by maintaining the relation CoPy = KG, for a constant K. Mean percentage of tau-guidance for all groups was ¸99%, resulting in all r² exceeding 0.95, justifying an investigation of the regression slope as an estimate of the coupling constant K in the tau-coupling equation. Mean K values decreased signiWcantly with age and were for 2- to 3-year-olds 0.56, for 4- to 5-year-olds 0.50, for 7- to 8-yearolds 0.47, and for adults 0.41. Therefore, the control of dynamic balance develops from the youngest children colliding with the boundaries of the base of support (K > 0.5) to the older children and adults making touch contact (K · 0.5). The Wndings may provide us with a measure for testing prospective balance control, a helpful tool in assessing whether a child is following a normal developmental pattern. Keywords Dynamic balance · Gait initiation · Movement control · Prospective control · Tau-G analysis · Children H. Austad · A. L. H. van der Meer (&) Developmental Neuroscience Laboratory, Department of Psychology, Norwegian University of Science and Technology (NTNU), Trondheim, Norway e-mail: [email protected] Introduction A major milestone in a child’s life is to no longer have to hold on to any of the surrounding surfaces to balance the body in an upright position and attain independent walk. In the process of achieving this, the child has to learn to use sensory information and motor action together to orient his or her presence in the environment. The child also has to be able to stabilize the body’s center of gravity (Barela et al. 1999), the point where the body is in perfect balance. Stable control of posture and balance is an integral component of all motor abilities (Ferdjallah et al. 2002). A common method for measuring postural stability is to obtain movement of center of pressure (CoP) data from force plates (Cherng et al. 2003). Independent walking is a highly complex series of actions. It changes style as we grow older and become more skilled walkers, and will, by adulthood, be characterized by smooth, regular, and repetitive movements (Vaughan 2003). The speciWc ankle displacement in mature walking, resulting in a prominent heel strike and push oV, is absent in new walkers (Dierick et al. 2004). Young children walk with a wide base of support. As they mature, they are better able to control their body weight over the supporting limb, due to greater coordination and improved balance (Sutherland 1997). The pelvic span/ankle spread ratio increases steadily from the beginning of walking until about the age of 3½ after which it remains constant. Age and more practice improve balance control, leading to better postural control and decreased postural sway (Rival et al. 2005). Some researchers have observed that children under the age of 4 have relatively longer steps than older children and adults when the step length is compared to leg length (Dierick et al. 2004; Sutherland 1997). New walkers also 123 Exp Brain Res use a high and middle guard posture of the arms which has been found to be correlated to step width, as well as a natural factor in helping to move the body forward at a time when the child’s muscles in the lower limbs are not strong enough to cause movement on their own (Kubo and Ulrich 2006; Ledebt 2000). Ledebt (2000) reported that children will lower their arms and progressively start moving them, Wrst in the shoulder joint, and then also the elbow, supporting Bernstein’s (1967) theory of initially freezing the redundant degrees of freedom in motor skill learning. Then, as the new skill is practiced, “freeing” of degrees of freedom allow more movement as new tasks are performed with less restrictions, while still maintaining body posture (Newell and Vaillancourt 2001). It is well known that adults prepare for the Wrst step, in part, by leaning forwards, which sets oV a controlled fall and the initiation of gait (Mann et al. 1979). When controlling posture and balance during gait, the task is to maintain the movement of the CoP within the boundaries of the base of support (MacKinnon and Winter 1993). Brenière and Bril (1998) found that young toddlers are not able to control the disequilibrium which characterizes the single support phase. Their study showed that during the Wrst 6 months of independent walking children displayed negative values of the vertical acceleration of the center of mass at foot contact, while adults displayed positive values. They concluded that toddlers can walk, despite lacking the strength required to maintain balance, but that they are “walking by falling”. It is not until the age of 4–5 years that children are able to control this fall by controlling gravity forces and the inertia forces induced by movement (Brenière and Bril 1998). Assaiante et al. (2000) studied the development of postural adjustment during gait initiation from kinetic and EMG as well as kinematic analyses. They reported that anticipatory postural adjustments that shift the weight towards the stance leg preceded the integrative postural adjustments that take care that balance is stabilized during the swing phase of gait when the body is supported by one leg. Both processes, however, did not mature before the age of approximately 4–5 years. A common problem in movement control is that of stabilizing an eVector within the boundaries of a goal zone. For example, in balance control this would involve stabilizing the vertical projection of the centre of gravity within the boundaries of the base of support. Movement can be described as a goal-directed action. The intention is to get from state A to state B, which necessitates the closure of the gap between the two states. The gap between the two states is called a motion-gap. Thinking of a step as the closure of a motion-gap leads to the theory, which will be used in this study, to estimate the prospective control of balance in the transitional stage between standing still and starting to walk: General tau theory (Lee 1998, 2005; Lee et al. 2001). 123 Tau, , of a motion-gap is the time it will take to close the gap at its current closure rate. A gap can be either a spatial or a force gap (Lee 1998). Lee (1998) writes that at the root of general tau theory is the idea of prospective control. The movement has to be controlled ahead of time to allow for such factors as inertia. Prospective guidance of a selfpaced movement (such as taking a step, or reaching for a stationary object) requires intrinsic information generated in the central nervous system and perceptual information, but it is not necessary to know the size of the gap, neither the rate of closure (Lee et al. 2001). It is, however, necessary to monitor the progress of the movement perceptually so that appropriate muscular adjustments can be made (Lee 2005), which in turn will minimize the risk of falling when walking (Vaughan 2003). Intrinsic tau guidance is goal-oriented, aiming at closing the motion-gap between the current state and the desired state. The dimension which underlies the process of change in any motion-gap is time, and it is necessary to be able to perceive the motion-gap and estimate the time it will take to close the motion-gap at the current closure rate without falling short of, or crashing into the target or goal state (Lee 2005; Slobounov et al. 1997). When used to guide a self-paced movement to a goal, the motion-tau would be constantly tau-coupled onto an intrinsic tau-G guide (Craig et al. 2000a). The general tau theory can be applied to any kind of gap closure. If we imagine an upright cylinder surrounding us when we walk, the walls of this cylinder can be thought of as guiding upright posture. When walking or running, the task is to control the movement of the CoP to stay within the walls of the cylinder, i.e., within the boundaries of the base of support. The present study This study investigated, by measuring the abilities of children in three diVerent age groups, the levels of postural control during the transitional stage between standing still and walking, i.e., when taking the initial step. The results were compared to those of an adult group. It was expected that as children become more skilled walkers, their control of the movement of the CoP would improve. It was postulated that controlling the movement of the CoP in the antero-posterior direction (CoPy) entails controlling the closure of the motion gap between the current position of the CoPy and a goal position lying within the cylinder; and that this is achieved by tau-G guiding the motion-gap, i.e., keeping the changing tau of the motion-gap proportional to an intrinsically generated changing tau value, tau-G. It was expected that the youngest children would overshoot the goal position (rather than making touch contact with it, as the oldest children and the adults would), because their tauG guidance of CoPy was underdeveloped. This study aimed to identify and map out the developmental stages of gait Exp Brain Res initiation so as to create a barometer for predicting prospective balance control, a helpful tool in assessing if a child is following a normal developmental pattern. Method Participants The children in this study were divided into three age groups: (1) 2- to 3-year-olds, mean age 2.9 years (§0.2), (2) 4- to 5-year-olds, mean age 4.8 years (§0.6), and (3) 7- to 8-year-olds, mean age 7.3 years (§0.2). A total of 21 children were recruited to participate in this study. However, only six children from each age group were analyzed due to technical problems (1), insuYcient data (1), and a history of ear infections (1). In addition, a total of six adults participated. The mean age for the adults was 27.8 years (§3.3). Each group consisted of four females and two males. Participants for the two youngest age groups were recruited from the University nursery where the parents of the children were given letters informing them about the research and requesting consent for their children to be brought to the Developmental Neuroscience Laboratory, Department of Psychology, Norwegian University of Science and Technology (NTNU), during the day, by a nursery worker. The 7- to 8-year-olds were recruited among friends’ children and their friends, and all were pupils at one of the primary schools nearby. All the adult participants were volunteers from master level classes in psychology. All child participants involved in this study were conWrmed born to term. None of the parents reported any developmental problems with balance or other motor control behaviors, vision or auditory problems, or anything else which could have an inXuence. All adult participants had normal or corrected to normal vision. One of the adults reported some childhood ear infections. None of the adult participants reported having experienced any motor control diYculties. Parents and adult participants gave their informed written consent prior to inclusion in the study according to the Helsinki Declaration. Apparatus and procedure Center of pressure data were collected using custom-built force plates. There were four plates (92 £ 83 cm each) lined up in a row, creating a walkway. The two plates in the middle were used for data collection. The force plate data were sampled at 100 Hz. In addition, all trials for all the participants were recorded on video. A trial consisted of a period where the participant was standing still, after which s/he was asked to walk across both force plates. The youngest children were looking after a raisin, which they had to put in a cup at the opposite end of the platform. The raisins were given as a reward at the end of the experiment. In addition, all children received a diploma for their participation. Each participant completed between 7 and 10 trials. The adult participants were given instructions at the beginning of the session and asked to adopt a quiet two-legged stance. They were also asked to start their walking with intention, as if they had a purpose with the walk across the force plates. All participants wore socks during testing. Data analysis The video recordings were inspected to extract from the data step initiation until the foot was placed back on the platform. Since walking occurs, to a large degree, in the antero-posterior direction, only movement of CoPy was analyzed for step initiation. The data were Wltered using a Gaussian sigma 3 Wlter. The displacement of CoPy and its velocity (rate of closure of CoPy motion-gap) were plotted against time (see Figs. 1b, 2b). The peak velocity of each Wrst step was identiWed and the movement of CoPy was demarcated at 10%, or as close to 10% as possible, of this value. The CoPy (i.e., the tau of the gap between the beginning and the end of the movement of CoPy) was calculated and plotted against the tau-G guide (G) for the movement, using the formula G(TG,t) = TG(1 + tn)tn/(1 + 2tn), where TG is the CoPy motion duration, which starts at time t = 0, for ¡TG · t · 0, or ¡1 · tn · 0 (Lee 2005). Finally, a recursive linear regression analysis was run on the plot to determine the strength of the coupling between CoPy and G (measured by the r² value of the regression) and to estimate the value of the constant K in the tau-coupling equation CoPy = KG (measured by the slope of the regression), by removing the leftmost points in the plot one by one until the r² of the regression exceeded the criterion level which was set at 0.95. The percentage of the movement during which it has intrinsic tau-G guidance was calculated by dividing the remaining points in the plot by the total number in the movement, providing an estimate of how much the CoPy movement was prospectively controlled. Thus, for the fragment identiWed in each movement three measures were given: (1) the percentage of the movement that was tau-G guided to the criterion of r² ¸ 0.95, (2) the value of r², and (3) the regression slope, which estimates the K value in the tau-coupling equation. High percentages of tau-G guidance of the movement and high r² values allow for the regression slope to be a good estimator of the K of the movement. The value of K in the tau-coupling equation regulates the kinematics of closure of the CoPy motion-gap. In particular, for K values lying between 0 and 1, the larger the value of K, the longer the duration of the acceleration phase of the 123 Exp Brain Res Start a End Start 80 80 60 60 Displacement of CoPy (cm) Displacement of CoPy (cm) a 40 20 0 -20 -40 40 20 0 -20 -40 -60 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 -60 1.6 0.0 Time (s) End 300 20 250 0 -10 200 Displacement of CoPy Velocity of CoPy 150 100 -20 -30 50 -40 0 0.2 0.4 0.6 0.8 Time (s) 1.0 1.2 Start 1.4 1.6 End 30 300 20 250 10 0 -10 200 Displacement of CoPy 150 Velocity of CoPy 100 -20 -30 50 -40 0 Velocity of CoPy (cm/s) 10 b Displacement of CoPy (cm) Start 30 Velocity of CoPy (cm/s) Displacement of CoPy (cm) b End -50 0.0 0.2 0.4 0.6 0.8 -50 0.0 Time (s) 0.2 0.4 0.6 0.8 Time (s) Fig. 1 a Displacement of CoPy during normal gait in a typical 2-yearold, where the CoPy oscillates between the medial borders of the supporting feet (dashed lines). The vertical solid lines mark the start and the end of the CoPy movement during gait initiation. b Zooming in on the displacement of CoPy and its corresponding velocity curve during the initial step. The resulting K value was 0.53, indicating that the movement of CoPy is colliding with the boundaries of the base of support movement and the more abrupt the deceleration to the goal (Lee 1998). The three ranges of K give rise to distinct types of movement (Lee 2005). When 0 < K · 0.5, the CoPy movement starts at rest and moves away with increasing acceleration from a zero value; the movement then decelerates at a decreasing rate and stops at the goal. Thus, when 0 < K · 0.5, the movement ends with touch contact. When 0.5 < K < 1, the CoPy movement starts at rest and moves away with a high initial acceleration, which decreases to zero. Then the movement decelerates at an increasing rate until maximum deceleration is achieved, which is maintained until the goal is reached. Thus, when 0.5 < K < 1, the movement ends with hard contact while the movement is decelerating. A controlled collision is the consequence. When K ¸ 1, the CoPy movement starts moving away at speed, decelerates at a decreasing rate and then accelerates at an increasing rate until maximum acceleration is achieved, and Wnally hits the goal at high velocity. 123 Fig. 2 a Displacement of CoPy during normal gait in a typical adult, where the CoPy oscillates between the medial borders of the supporting feet (dashed lines). The vertical solid lines mark the start and the end of the CoPy movement during gait initiation. b Zooming in on the displacement of CoPy and its corresponding velocity curve during the initial step. The resulting K value was 0.41, indicating that the movement of CoPy is heading for the boundaries of the base of support with touch contact The eVect is a non-controlled collision. So, K values greater than one indicate that the movement is still accelerating when it reaches its goal. Results A total of 202 trials were recorded. One of these was deWned as an outlier [value larger/smaller than mean §2.5 SD, see Field (2005)] and was therefore excluded from the analysis. Figure 1a illustrates the displacement of CoPy during gait in a typical 2-year-old, and Fig. 1b zooms in on the initial step and illustrates displacement of CoPy and its corresponding velocity during gait initiation until the swinging foot is placed back on the force plate. Figures 2a and b show the same for a typical adult. Exp Brain Res Tau-G analyses The percentage of tau-G guidance of the CoPy movement was close to 100% in most of the trials. The mean percentage of tau-G guidance was for the 2- to 3-year-olds 99.54%, for the 4- to 5-year-olds 99.77%, and 100% for both the 7- to 8-year-olds and the adults, which resulted in all the r² exceeding 0.95, indicating that the tau of CoPy was strongly coupled onto the tau-G guide. Therefore, further analysis was only performed on the K values, which show how well the movement of CoPy was controlled. Group mean K values (see Fig. 3) were for the 2- to 3-year-olds 0.56 (range 0.51–0.67), for the 4- to 5-year-olds 0.50 (range 0.46–0.51), for the 7- to 8-year-olds 0.47 (range 0.44–0.48), and for the adults 0.41 (range 0.39–0.44). A one-way ANOVA with group as between factor was carried out on the subject means of the K values, revealing a main eVect of group, F(3, 20) = 11.02, P < 0.001, indicating lower K values with increasing age. A linear regression analysis performed to get an estimate of change of the mean K value with age revealed an r² of 0.57 and a standardized correlation coeYcient of ¡0.75 (t = ¡5.36, P < 0.001). The subject mean K values were tested with a one sample t test to see if the results were signiWcantly higher or lower than 0.5 (see Fig. 3). The 2- to 3-year-olds had K values signiWcantly higher than 0.5, which means that the youngest children collided with the boundaries of the base of support (K > 0.5). Both the 7- to 8-year-olds and the adults had K values signiWcantly lower than 0.5, which means that they made touch contact with the boundaries of the base of support (K · 0.5). The 4- to 5-year-olds did not 0.7 K>0.5, p<0.03 Me an K valu e 0.6 K<0.5, p<0.001 0.5 K<0.5, p<0.001 0.4 0.3 2-3 years 4-5 years 7-8 years Adults Fig. 3 Group means (and error bars) of the K values of the CoPy movement during the Wrst step. The 2- to 3-year-olds had K values signiWcantly larger than 0.5, whereas the 7- to 8-year-olds and the adults had K values signiWcantly smaller than 0.5. The 4- to 5-year-olds had K values that were not signiWcantly diVerent from 0.5. The horizontal line indicates K = 0.5, demarcating the switch from making a controlled collision with the boundaries of the base of support (K > 0.5) to making touch contact (K · 0.5) have K values signiWcantly diVerent from 0.5, placing them somewhere between the 2- to 3-year-olds and the 7- to 8-year-olds. Typical for the 4- to 5-year-olds was that they all had K values hovering around 0.5, with K · 0.5 in just over half of the trials (55%). The corresponding percentages for the 2- to 3-year-olds, the 7- to 8-year-olds, and the adults were 34, 78, and 100%, respectively. Discussion This study investigated the development of postural control during gait initiation in healthy children aged 2–3, 4–5, and 7–8 years, as well as in a group of adult graduate studentvolunteers. This study, contrary to many other studies carried out on balance control (Assaiante and Amblard 1992; Cherng et al. 2003; Ferdjallah et al. 2002; Hatzitaki et al. 2002; Jeka et al. 2000; Peterson et al. 2006), included no manipulations. To study postural control, the movement of CoPy was tau-G analyzed during the Wrst step when gait was initiated. The percentage of total tau-G guidance for the movement was higher than 99% which meant that all the r² exceeded 0.95. The resulting K values gave an indication of how well movement of CoPy was controlled. K values decreased signiWcantly with age, and the control of dynamic balance during the Wrst step when gait is initiated, showed a development from the youngest children colliding with the boundaries of the base of support (K > 0.5) to the oldest children and the adults making touch contact (K · 0.5). The present Wndings indicated that the youngest children have the least control over their movements in dynamic balance. When K > 0.5 the control of the movement is very diVerent from that when K · 0.5. If we imagine an upright cylinder surrounding us when we walk, the walls of this cylinder can be thought of as guiding upright posture. We can imagine the youngest children overshooting the goal position lying within the cylinder and colliding with its wall when they start walking, but not so hard that they topple over and fall. The oldest children and the adults, in the same scenario, will just make touch contact with the wall when they initiate walking. It has previously been found that children up to the age of 4–5 years do not show integrative postural adjustment, which keeps the pelvis from dropping to the side of the swing leg during foot liftoV. The result is a balance problem for the youngest children during the swing phase of gait (Assaiante et al. 2000). This is consistent with another study of young children where it was found that gait was a result of “walking by falling” (Brenière and Bril 1998). It has been proposed that around the age of 6–7 years, a recalibration of the sensory processes underlying locomotor balance control takes place 123 Exp Brain Res due to a growth spurt in the trunk, which causes a sudden shift in the center of gravity. From the age of 7–8 years onwards the visual, vestibular, and proprioceptive systems become more eYciently coordinated, resulting in improved dynamic balance control (Assaiante and Amblard 1992). Based on this, the tau-G analysis yielded similar results as other researchers have reported, and the coupling constant K in the tau-coupling equation gives a good indication of the diVerences in control between the age groups when initiating gait. It should be mentioned that the task for the youngest children was slightly diVerent than for the other participants. In order to engage the youngest children in the task they were asked to carefully look after a raisin and place it in a cup at the end of the platform. Although the 2- to 3-year-olds appeared to take this task very seriously, most likely resulting in more cautious gait initiation, it cannot be entirely ruled out that the higher K values were a result of the youngest children being excited about the raisin game causing them to hurriedly take the Wrst step. It has been demonstrated here that intrinsic tau-G analysis can successfully be applied to the study of dynamic balance control. The present study is actually the Wrst study to take CoP measurements from children during the Wrst step in gait initiation and apply the general tau theory. However, the theory has successfully been applied to other tau-coupling situations, e.g., when studying how professional golfers control the swing of the golf club when putting (Craig et al. 2000a) and how children with hemiparetic cerebral palsy (CP) control their hitting movements (Van der Weel et al. 1996). Tau-coupling was also used to analyze nutritive sucking in healthy infants (Craig and Lee 1999). Those results were compared to results obtained from preterm infants (Craig et al. 2000b). The results revealed that some preterm infants displayed irregularities in sucking control and when compared to an independent physiotherapist’s assessment 6 months later, the same preterm infants were found to be delayed in their motor development. These Wndings suggest that tau-G analysis can be used as a diagnostic tool. Many studies have been carried out with both adults and children suVering developmental delays, or set-backs, caused by disease or events. A common component between all these studies is that they have used the measure of CoP to determine the degree of stability. For example, in studies with patients diagnosed with Parkinson’s disease (e.g., Guehl et al. 2006) intrinsic tau-G analysis could be added, allowing the researchers to study the control of the CoP movements as well as their position, displacement, and area. Other postural control studies where the use of intrinsic tau-G analysis could prove valuable is in the search for better recovery treatment after stroke (e.g., Bayouk et al. 2006), and the treatment of children with developmental 123 coordination disorders (DCD), CP, and idiopathic scoliosis (e.g., Bennett et al. 2004). Based on the Wndings from the preterm infants study (Craig et al. 2000b) as well as the results from the present study, tau-G analysis applied to motor development studies seems promising. The analysis would appear to give a good indication of the level of temporal control involved in performing a movement of the CoP when initiating gait, as well as diVerentiate between diVerent developmental stages. More studies should be carried out to establish baselines for motor control development in healthy children in more age groups, followed by using similar methods to evaluate the development levels reached by children with developmental disorders. The ability to estimate prospective control makes tau-G analysis a useful tool in studying developmental delay problems and motor control deWciencies, possibly making treatment and intervention more accurate. Acknowledgments The research reported in this paper was part of a Master’s thesis by H. Austad. 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