Gait & Posture 40 (2014) 32–37
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Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Effect of Achilles tendon vibration on posture in children Sandra M. McKay a, Jianhua Wu b,*, Rosa M. Angulo-Barroso c,d a
Centre for Studies in Aging, Sunnybrook Health Sciences Centre, Toronto, ON, Canada Department of Kinesiology and Health, Georgia State University, Atlanta, GA, USA c Center for Human Growth and Development, University of Michigan, Ann Arbor, MI, USA d INEFC, Department of Health and Applied Sciences, University of Barcelona, Barcelona, Spain b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 May 2013 Received in revised form 31 January 2014 Accepted 7 February 2014
This study investigated the effect of unilateral Achilles tendon vibration on postural response in children and young adults during standing. Thirty healthy subjects participated in this study including ten 6year-old children (YC group), ten 10-year-old children (OC group), and ten young adults (YA group). Eight-second vibration was elicited in each trial from a small vibrator attached above the right Achilles tendon when participants stood barefoot on a force platform. Three 40-s trials were collected under both eyes-open and eyes-closed conditions. Center of pressure (COP) was calculated to examine postural response during the pre-vibration, vibration and post-vibration phases. Results show that both the YC and OC groups had a greater COP average velocity than the YA group in all three phases. Tendon vibration induced a directionally specific postural response in all three groups such that the onset of vibration induced a posterior and medial COP shift during the vibration phase, and the offset of vibration induced an anterior and lateral COP shift during the post-vibration phase. Timing of the maximal COP shift was comparable among three groups in both anterior–posterior (AP) and medial–lateral (ML) directions. However, only the OC group showed an adult-like magnitude of the maximal COP shift during the postvibration phase in the AP direction. These results suggest that 6-year-old children may start showing an adult-like directionally specific response and temporal parameter to tendon vibration during standing; however, the development of an adult-like spatial postural response to tendon vibration may take more than 10 years. Published by Elsevier B.V.
Keywords: Posture Children Achilles tendon vibration Center of pressure
1. Introduction Maintaining an upright stance is affected by sensory information received from the visual, vestibular and somatosensory systems. The integration of sensory information is necessary during standing when the sensory inputs from one or more of these sensory systems are altered. One can manipulate visual input by occluding visual input or providing a movable visual surround, and alter the somatosensory information by using a translating or tilting platform [1,2]. These experimental settings have been used to understand postural development in children [3–5]. However, it is still not in consensus about the time course of postural development in children. For instance, children at 8 years of age show adult-like postural sway velocity during standing with and without visual input [4]. When both visual and somatosensory information are altered, children at 7 years of age display adult-like
* Corresponding author. Tel.: +1 404 413 8476; fax: +1 404 413 8053. E-mail address: [email protected] (J. Wu). http://dx.doi.org/10.1016/j.gaitpost.2014.02.002 0966-6362/Published by Elsevier B.V.
muscle activation during standing [1,6]. However, other evidence suggests that somatosensory function may be comparable to the adult level at 4 years of age during postural tasks, but the integration of visual and somatosensory information may not reach the adult level until 15 years of age [7,8]. Applying mechanical vibration to muscle tendons is another method to altering proprioceptive information during human movement. Vibration on the tendon of quadriceps induces a knee extension [9] while vibration on the tendon of biceps induces an elbow flexion [10]. It is generally recognized that tendon vibration induces stretches of muscle spindles and the higher neural centers interpret this as an increased muscle spindle discharge due to muscle lengthening, resulting in the contraction of the vibrated muscle to produce a direction-specific postural response [9–11]. Direction specificity depends on the placement of tendon vibration during standing tasks. For instance, bilateral vibration on the Achilles tendons induces a backward body tilt [12–18], whereas bilateral vibration on the tendons of tibialis anterior induces a forward body tilt [15–17]. Unilateral vibration on the right Achilles tendon induces not only a backward body tilt, but also a medial
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body shift during standing [19]. On the other hand, the termination of tendon vibration causes body tilt in the opposite direction beyond the initial standing position [16,20]. Other evidence suggests that there may be either an overcorrection or an undercorrection to the initial standing position immediately after tendon vibration is terminated [21]. In contrast to the extensive literature on tendon vibration in adults, limited research has been conducted by using this experimental paradigm with children. A recent study applied bilateral vibration on both the Achilles and tibialis anterior tendons in children at 7–11 years of age while standing in a tandem position [22]. It was found that children produced a greater velocity of postural sway in the medial–lateral direction than adults; however, a marked improvement was seen in children at 10 years of age. To our knowledge, no study has investigated the effect of the onset and offset of tendon vibration on postural control in children. Studying the onset of tendon vibration will reveal the initial response of children to vibrational perturbation during standing, while studying the offset of vibration will shed light on the post-effect of vibration on postural control. The purpose of this study was to investigate postural response in 6- and 10-year-old children while adapting to the altered visual and proprioceptive information during standing. We manipulated the proprioceptive information via tendon vibration and altered the visual information via vision occlusion. Because children at 6 and 10 years of age display an adult-like strategy to regulate variability but still show a higher magnitude of variability during quiet standing [23], we hypothesized that 6-year-old children may start showing an adultlike direction-specific postural response to unilateral Achilles tendon vibration, but the magnitude of response may not reach the adult level even in 10-year-old children.
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tendon. The outer casing of the motor was marked on the subject’s skin and checked periodically through the testing session to ensure the same placement. A pressure-sensing resistor (Interlink Electronics, Camarillo, CA) was placed between the Achilles tendon and the motor to provide an objective measure of pressure applied by the motor and helped standardize the attachment tension. Amplitude of vibration was found to dampen as much as 75 percent following tendon attachment to an individual [26]. Analysis of the pressure data from our first and last standing trials verified that each participant received the same stimulation applied by the motor across trials and groups. Participants stood barefoot on a Bertec 4060A force platform (Bertec, Columbus, OH) with their hands comfortably on the iliac crests. Kinetic data were collected by the force platform at a sampling rate of 600 Hz. Participants were instructed to maintain their normal standing posture while neither aligning their body rigidly nor swaying their body intentionally. The force platform was covered with a piece of brown butcher paper on which the feet were marked to ensure the same foot position throughout the data collection. Each standing trial lasted 40 s. The first 10 s were quiet standing without vibration and then vibration was triggered whenever the criterion was met. The criterion was that the force in the anterior–posterior (AP) axis was pointing to the anterior
[(Fig._1)TD$IG]
2. Methods 2.1. Participants Thirty healthy individuals participated in this study: younger children (YC, n = 10), older children (OC, n = 10), and young adults (YA, n = 10). Table 1 presents the physical characteristics of these participants. All the participants reported that they were free of any neuromuscular injuries or neurological disorders that would affect their ability in maintaining stable posture during standing. This study was approved by the Institutional Review Board at the University of Michigan. All the participants and the parents of the YC and OC groups gave written informed consent before participation. 2.2. Data collection A small wave pulse motor with an eccentric mass was used to stimulate the right Achilles tendon at 80 Hz [15,17,24,25]. The motor was measured 7 cm in length, 4 cm in width, and weighed 127.6 g. The motor was contained within a plastic cylinder with a concave surface to accommodate placement over the Achilles Table 1 Mean (SD) of the participant characteristics.
Gender Age (year) Body mass (kg) Height (cm) BOS_AP (cm) BOS_ML (cm)
YC
OC
5F/5M 6.33 (0.59) 20.80 (4.10) 114.10 (6.52) 18.56 (1.72) 24.96 (3.95)
6F/4M 10.33 (0.92) 35.30 (8.32) 137.05 (8.48) 21.46 (1.96) 25.10 (3.41)
YA 8F/2M 20.50 (1.39) 62.21 (11.01) 165.70 (8.86) 24.47 (1.60) 29.14 (2.75)
YC—younger children; OC—older children; YA—young adults; BOS—base of support; AP—anterior–posterior; ML—medial–lateral.
Fig. 1. A representative COP trajectory from a YA subject. The trajectory includes 5 s before the vibration onset (pre-vibration phase), 8 s of vibration (vibration phase), and 5 s after the vibration offset (post-vibration phase). Two vertical gray broken lines represent the vibration onset and offset, respectively. Timing of 0 s was the vibration onset and the vibration lasted for 8 s. (a) Anterior displacement was positive and posterior displacement was negative in the anterior–posterior (AP) direction. (b) Medial displacement was positive and lateral displacement was negative in the medial–lateral (ML) direction. The ML and AP directions were the xaxis and y-axis of the force platform, respectively.
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direction and the moment about the medial–lateral (ML) axis was causing an anterior rotation. The 8-s vibration was chosen to induce postural response in an optimal time window [19]. Two visual conditions were examined including eyes-open (EO) and eyes-closed (EC). In the EO condition, participants fixated a poster hung on the wall at their eye level about two meters away. In the EC condition, participants closed their eyes during each trial. Three 40-s trials were collected in each condition. The order of trials was randomized across the participants. Enough rest was provided between trials to minimize fatigue, particularly in younger children. Standing trials without tendon vibration were also collected and reported elsewhere [23]. 2.3. Data analysis Center of pressure (COP) data were analyzed in the AP and ML directions separately. Due to the differences in physical characteristics among three groups (such as base of support (BOS) in Table 1), COP data in the AP and ML directions were normalized to each participant’s BOS_AP and BOS_ML measures, respectively. Three phases of each standing trial were examined: 5 s before the vibration onset (pre-vibration phase), 8 s of vibration (vibration phase), and 5 s after the vibration offset (post-vibration phase). Average velocity was calculated as total excursion of the COP movement divided by the duration in each phase [27]. The Achilles tendon vibration at the right ankle induced the COP shifts in both the AP and ML directions. In the AP direction, the vibration onset induced a posterior COP shift and the vibration offset induced an anterior COP shift (Fig. 1a). In the ML direction, the vibration onset induced a medial COP shift and the vibration offset induced a lateral COP shift (Fig. 1b). The maximal COP shifts after the vibration onset and offset were considered to be the vulnerable positions which may cause a loss of balance. Therefore, the maximal posterior and medial COP shifts were examined after
[(Fig._2)TD$IG]
the vibration onset in the AP and ML directions, respectively, during the vibration phase. The maximal anterior and lateral COP shifts were examined after the vibration offset in the AP and ML directions, respectively, during the post-vibration phase. Timing of the maximal COP shift was determined as latency in seconds after the vibration onset during the vibration phase and latency in seconds after the vibration offset during the post-vibration phase. Mean COP position during the pre-vibration phase was used as the baseline when calculating the magnitude of the maximal COP shift. 2.4. Statistical analysis A series of 3 (Group) 2 (Visual) 3 (Phase) ANOVA with repeated measures on the last two factors were conducted on COP average velocity for all three phases in both the AP and ML directions. A series of 3 (Group) 2 (Visual) 2 (Phase) with repeated measures on the last two factors were conducted on the timing and magnitude of each maximal COP shift to compare the vibration and post-vibration phases. Absolute values of these magnitudes were used for this analysis while the original magnitudes were presented in Fig. 3. All the statistical analyses were performed using SAS software version 9.2 (SAS, Cary, NC). Significance level was set as p < 0.05. Post-hoc comparisons with Bonferroni adjustments were conducted when appropriate. 3. Results 3.1. COP average velocity In the AP direction, there was a group by phase interaction (p = 0.0219) and a visual by phase interaction (p = 0.0260) (Fig. 2a and c, Table 2). While all three groups increased average velocity from the pre-vibration phase to both vibration and post-vibration phases, both the YC and OC groups increased this variable to a greater extent than the YA group. The YC group produced a higher average velocity than the OC group, who produced a higher velocity than the YA group, during each phase. Compared to average velocity in the EO condition, the EC condition
Fig. 2. Mean and standard deviation of the COP average velocity. (a) In the EO condition and AP direction, (b) in the EO condition and ML direction, (c) in the EC condition and AP direction, and (d) in the EC condition and ML direction. Average velocity was normalized to the subjects’ base of support in the AP and ML directions, respectively. BOS_AP, base of support in the AP direction; BOS_ML, base of support in the ML direction; EO, eyes open; EC, eyes closed.
p = 0.2693 p = 0.9646 p = 0.5677 p = 0.6732 F(2,27) = 1.38, F(2,27) = 0.04, F(2,27) = 0.58, F(2,27) = 0.40, p = 0.6901 p = 0.8682 p = 0.9306 p = 0.5275 F(1,27) = 0.16, F(1,27) = 0.03, F(1,27) = 0.01, F(1,27) = 0.41,
F(1,27) = 51.30, p < 0.0001 F(1,27) = 13.08, p = 0.0012
F(1,27) = 1.58, p = 0.2195 F(1,27) = 15.64, p = 0.0005 F(1,27) = 1.07, p = 0.3098 F(1,27) = 4.33, p = 0.0472 F(2,27) = 2.19, p = 0.1315 F(2,27) = 36.38, p < 0.0001 F(2,27) = 2.31, p = 0.1187 F(2,27) = 11.31, p = 0.0003
Average velocity AP ML Maximal COP shift Timing: AP Magnitude: AP Timing: ML Magnitude: ML
F(2,27) = 43.28, p < 0.0001 F(2,27) = 23.05, p < 0.0001
p = 0.8705 p = 0.3677 p = 0.1218 p = 0.6096
F(2,27) = 3.10, F(2,27) = 5.00, F(2,27) = 0.59, F(2,27) = 4.04,
p = 0.0615 p = 0.0143 p = 0.5591 p = 0.0292 F(2,27) = 0.14, F(2,27) = 1.04, F(2,27) = 2.28, F(2,27) = 0.50, F(1,27) = 119.48, p < 0.0001 F(1,27) = 11.41, p = 0.0002 F(1,27) = 52.34, p < 0.0001 F(1,27) = 27.67, p < 0.0001
F(4,54) = 0.31, p = 0.8671 F(4,54) = 0.68, p = 0.6089 F(2,54) = 3.91, p = 0.0260 F(2,54) = 2.25, p = 0.1148 F(4,54) = 3.13, p = 0.0219 F(4,54) = 3.07, p = 0.0237 F(2,27) = 0.94, p = 0.4047 F(2,27) = 0.86, p = 0.4350 F(2,54) = 31.02, p < 0.0001 F(2,54) = 24.52, p < 0.0001
Group Visual Phase Group Phase Group
Table 2 Statistical results of the COP variables.
Visual
Phase
Group Visual
Visual Phase
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marginally increased average velocity during the pre-vibration phase, but significantly increased it during both vibration and post-vibration phases across all three groups. In the ML direction, there was a group by phase interaction (p = 0.0237) and a visual effect (p = 0.0012) (Fig. 2b and d, Table 2). Among the three phases of standing trials, both the YC and OC groups showed the greatest average velocity during the vibration phase and the smallest values during the pre-vibration phase. In contrast, the YA group had a similar average velocity across the three phases. The YC group produced a higher average velocity than the OC group, who produced a higher velocity than the YA group, during each phase. From the EO to the EC condition, all three groups increased average velocity. 3.2. Maximal COP shifts In the AP direction, there was a phase effect (p < 0.0001) on the timing of the maximal COP shift (Fig. 3a, Table 2). Across three groups and two visual conditions, mean timing of the maximal posterior shift during the vibration phase was 4.95 s after the vibration onset, and mean timing of the maximal anterior shift during the post-vibration phase was 2.85 s after the vibration offset. Also, there was a group by phase interaction (p = 0.0143) and a visual effect (p = 0.0005) on the magnitude of the maximal COP shift (Fig. 3b, Table 2). While the YC group had a similar magnitude between the vibration and post-vibration phases, both the OC and YA groups had a greater magnitude during the vibration phase than during the postvibration phase. The YC group had a greater magnitude than the OC and YA groups in both phases, whereas the OC group had a greater magnitude than the YA group only during the vibration phase. All three groups increased the magnitude of the maximal COP shifts from the EO to the EC condition during both vibration and postvibration phases. In the ML direction, there was a phase effect (p < 0.0001) on the timing of the maximal COP shift (Fig. 3c, Table 2). Across three groups and two visual conditions, mean timing of the maximal medial shift during the vibration phase was 4.50 s after the vibration onset, and mean timing of the maximal lateral shift during the postvibration phase was 2.88 s after the vibration offset. Also, there was a group by phase interaction (p = 0.0292) and a visual effect (p = 0.0472) on the magnitude of the maximal COP shift (Fig. 3d, Table 2). Both the YC and OC groups produced a greater magnitude during the vibration phase than during the post-vibration phase, whereas the YA group had a similar magnitude between the two phases. Both the YC and OC groups produced a greater magnitude than the YA group during the two phases. All three groups increased the magnitude of the maximal COP shifts from the EO to the EC condition during both vibration and post-vibration phases.
4. Discussion Both the YC and OC groups showed an adult-like directionspecific postural response to the Achilles tendon vibration above the right ankle during standing, i.e., a posterior COP shift in the AP direction and a medial shift in the ML direction after the onset of vibration, and an anterior COP shift in the AP direction and a lateral shift in the ML direction after the offset of vibration [16,19]. This finding suggests that children as young as 6 years of age develop an adult-like direction-specific postural strategy to respond to unilateral Achilles tendon vibration during standing. It implies that muscle spindles of gastrocnemius are sensitive to the Achilles tendon vibration in children as young as 6 years of age, and the increased discharge of these muscle spindles may induce the central nervous system to produce a directionally appropriate postural response. This finding is consistent with previous studies that children as young as 4 years show some adult-like somatosensory function during various standing tasks, but the maturation of the sensory systems continues until adolescence [7,8]. A greater COP average velocity in both the YC and OC groups suggests that regulation of postural sway velocity while adapting to unilateral tendon vibration may have not reached the adult level by 10 years of age. The OC group produced an adult-like response pattern in the AP direction such that the magnitude of the maximal COP shift was greater during the vibration phase than during the post-vibration phase. Further, the OC group displayed an adult-like magnitude of the maximal anterior COP shift during the postvibration phase in the AP direction. However, no adult-like response was observed from the OC group in the ML direction. These findings suggest that children at 10 years of age may not be able to concurrently regulate the COP movement in both the AP
[(Fig._3)TD$IG]
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Fig. 3. Mean and standard deviation of the timing and magnitude of the maximal COP shifts during the vibration and post-vibration phases. (a) Timing of the maximal posterior COP shift during vibration (in seconds after the vibration onset) and the maximal anterior COP shift during post-vibration (in seconds after the vibration offset) in the AP direction, (b) magnitude of the maximal posterior COP shift during vibration and the maximal anterior COP shift during post-vibration in the AP direction (posterior shift was negative and anterior shift was positive; normalized to the subjects’ BOS_AP measures), (c) timing of the maximal medial COP shift during vibration (in seconds after the vibration onset) and the maximal lateral COP shift during post-vibration (in seconds after the vibration offset) in the ML direction, and (d) magnitude of the maximal medial COP shift during vibration and the maximal lateral COP shift during post-vibration in the ML direction (medial shift was positive and lateral shift was negative; normalized to the subjects’ BOS_ML measures).
and ML directions while adapting to the right Achilles tendon vibration. Because a unilateral tendon vibration induces a greater COP shift in the AP direction than in the ML direction, children at 10 years of age may have to prioritize their response in the AP direction in order to avoid a loss of balance in this direction. This finding is consistent with our previous study in quiet standing such that children at both 6 and 10 years of age displayed an adult-like variability-partitioning strategy, but an adult-like magnitude of variability was not observed even in children at 10 years of age [23]. Taken together, we propose that there may be a two-phase postural development for both quiet and perturbed standing such that an adult-like direction-specific postural strategy develops first around 6 years of age and then a refinement process of magnitude regulation may continue beyond 10 years of age [5,28,29]. Both the YC and OC groups showed similar timings of the maximal COP shifts compared to the YA group, but only the OC group displayed an adult-like magnitude of the maximal anterior COP shift during the post-vibration phase in the AP direction while adapting to tendon vibration. This suggests that children as young as 6 years of age may have developed an adult-like temporal regulation of postural response, but an advanced spatial regulation may take more than 10 years to develop. This finding is consistent with the development of spatial and temporal parameters on pointing tasks in children at 7–10 years of age [30]. Previous studies also reported a similar temporal and spatial observation in EMG data such that children at 7–10 years of age show an adultlike EMG latency in gastrocnemius for a backward support surface translation and in tibialis anterior for a forward support surface translation, but may continue to develop the structural organization of muscle synergy between proximal and distal muscles as well as between agonist and antagonist muscles [1,6]. However, a
previous study using a backward support surface translation found that children at 7–10 years of age display adult-like spatial parameters such as peak COP amplitude and velocity, but not temporal parameters such as the timing of the COP peak [8]. Despite the inconsistent observations, all of previous studies suggest that control of spatial and temporal parameters for motor tasks may develop separately, which may involve distinct neural circuits and muscular systems and may be context dependent. Although the Achilles tendon vibration induces a backward postural sway just like a backward support surface translation, the integration of the sensory information may be different. While the Achilles tendon vibration mostly affects the spindle primary endings of gastrocnemius [11], a backward support surface translation may influence the plantar cutaneous information as well as other sensory messages from joint receptors and the vestibular system [1]. Given the inconsistent observations in spatial and temporal postural parameters in children, future studies, particularly with a longitudinal design, are warranted to reveal the time course of spatial and temporal development in various contexts of postural tasks. All three groups produced an anterior COP shift in the AP direction and a lateral shift in the ML direction after the offset of vibration, with respect to their mean COP position before the onset of vibration. This overcorrection response is consistent with the studies using a bilateral Achilles tendon vibration [16,20]. However, a previous study reported that bilateral Achilles tendon vibration induces both overcorrection and undercorrection responses, and the trunk orientation and pelvis tilt angle are different between these two responses [21]. Future studies are needed to investigate the orientation of body segments and leg muscle activation patterns in children while adapting to tendon
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vibration, which will help reveal the underlying kinematic and neuromuscular control strategies. Acknowledgments The authors are grateful to all the participants and their families for their participation in this study. Conflict of interest statement No author has any financial or personal relationship with other people or organizations that could inappropriately influence this work. References [1] Forssberg H, Nashner LM. Ontogenetic development of postural control in man: adaptation to altered support and visual conditions during stance. J Neurosci 1982;2:545–52. [2] Nashner L, Black F, Wall C. Adaptation to altered support and visual conditions during stance: patients with vestibular deficits. J Neurosci 1982;2:536–44. [3] Peterson ML, Christou E, Rosengren KS. Children achieve adult-like sensory integration during stance at 12-years-old. Gait Posture 2006;23:455–63. [4] Riach CL, Starkes JL. Velocity of center of pressure excursions as an indicator of postural control systems in children. Gait Posture 1994;2:167–72. [5] Schmid M, Conforto S, Lopez L, Renzi P, D’Alessio T. The development of postural strategies in children: a factorial design study. J NeuroEng Rehabil 2005;2:29. [6] Shumway-Cook A, Woollacott MH. The growth of stability: postural control from a developmental perspective. J Mot Behav 1985;17:131–47. [7] Hirabayashi SI, Iwasaki Y. Developmental perspective of sensory organization on postural control. Brain Dev 1995;17:111–3. [8] Peterka RJ, Black F. Age-related changes in human postural control: sensory organization tests. J Vestib Res 1990;1:73–85. [9] Eklund G. Position sense and state of contraction: the effects of vibration. J Neurol Neurosurg Psychiatry 1972;35:606–11. [10] Goodwin GM, McCloskey DI, Matthews PBC. Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science 1972;175:1382–4. [11] Roll JP, Vedel JP. Kinaesthtic role of muscle afferents in man, studied by tendon vibration and microneurography. Exp Brain Res 1982;47:177–90.
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Contents lists available at ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Effect of Achilles tendon vibration on posture in children Sandra M. McKay a, Jianhua Wu b,*, Rosa M. Angulo-Barroso c,d a
Centre for Studies in Aging, Sunnybrook Health Sciences Centre, Toronto, ON, Canada Department of Kinesiology and Health, Georgia State University, Atlanta, GA, USA c Center for Human Growth and Development, University of Michigan, Ann Arbor, MI, USA d INEFC, Department of Health and Applied Sciences, University of Barcelona, Barcelona, Spain b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 2 May 2013 Received in revised form 31 January 2014 Accepted 7 February 2014
This study investigated the effect of unilateral Achilles tendon vibration on postural response in children and young adults during standing. Thirty healthy subjects participated in this study including ten 6year-old children (YC group), ten 10-year-old children (OC group), and ten young adults (YA group). Eight-second vibration was elicited in each trial from a small vibrator attached above the right Achilles tendon when participants stood barefoot on a force platform. Three 40-s trials were collected under both eyes-open and eyes-closed conditions. Center of pressure (COP) was calculated to examine postural response during the pre-vibration, vibration and post-vibration phases. Results show that both the YC and OC groups had a greater COP average velocity than the YA group in all three phases. Tendon vibration induced a directionally specific postural response in all three groups such that the onset of vibration induced a posterior and medial COP shift during the vibration phase, and the offset of vibration induced an anterior and lateral COP shift during the post-vibration phase. Timing of the maximal COP shift was comparable among three groups in both anterior–posterior (AP) and medial–lateral (ML) directions. However, only the OC group showed an adult-like magnitude of the maximal COP shift during the postvibration phase in the AP direction. These results suggest that 6-year-old children may start showing an adult-like directionally specific response and temporal parameter to tendon vibration during standing; however, the development of an adult-like spatial postural response to tendon vibration may take more than 10 years. Published by Elsevier B.V.
Keywords: Posture Children Achilles tendon vibration Center of pressure
1. Introduction Maintaining an upright stance is affected by sensory information received from the visual, vestibular and somatosensory systems. The integration of sensory information is necessary during standing when the sensory inputs from one or more of these sensory systems are altered. One can manipulate visual input by occluding visual input or providing a movable visual surround, and alter the somatosensory information by using a translating or tilting platform [1,2]. These experimental settings have been used to understand postural development in children [3–5]. However, it is still not in consensus about the time course of postural development in children. For instance, children at 8 years of age show adult-like postural sway velocity during standing with and without visual input [4]. When both visual and somatosensory information are altered, children at 7 years of age display adult-like
* Corresponding author. Tel.: +1 404 413 8476; fax: +1 404 413 8053. E-mail address: [email protected] (J. Wu). http://dx.doi.org/10.1016/j.gaitpost.2014.02.002 0966-6362/Published by Elsevier B.V.
muscle activation during standing [1,6]. However, other evidence suggests that somatosensory function may be comparable to the adult level at 4 years of age during postural tasks, but the integration of visual and somatosensory information may not reach the adult level until 15 years of age [7,8]. Applying mechanical vibration to muscle tendons is another method to altering proprioceptive information during human movement. Vibration on the tendon of quadriceps induces a knee extension [9] while vibration on the tendon of biceps induces an elbow flexion [10]. It is generally recognized that tendon vibration induces stretches of muscle spindles and the higher neural centers interpret this as an increased muscle spindle discharge due to muscle lengthening, resulting in the contraction of the vibrated muscle to produce a direction-specific postural response [9–11]. Direction specificity depends on the placement of tendon vibration during standing tasks. For instance, bilateral vibration on the Achilles tendons induces a backward body tilt [12–18], whereas bilateral vibration on the tendons of tibialis anterior induces a forward body tilt [15–17]. Unilateral vibration on the right Achilles tendon induces not only a backward body tilt, but also a medial
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body shift during standing [19]. On the other hand, the termination of tendon vibration causes body tilt in the opposite direction beyond the initial standing position [16,20]. Other evidence suggests that there may be either an overcorrection or an undercorrection to the initial standing position immediately after tendon vibration is terminated [21]. In contrast to the extensive literature on tendon vibration in adults, limited research has been conducted by using this experimental paradigm with children. A recent study applied bilateral vibration on both the Achilles and tibialis anterior tendons in children at 7–11 years of age while standing in a tandem position [22]. It was found that children produced a greater velocity of postural sway in the medial–lateral direction than adults; however, a marked improvement was seen in children at 10 years of age. To our knowledge, no study has investigated the effect of the onset and offset of tendon vibration on postural control in children. Studying the onset of tendon vibration will reveal the initial response of children to vibrational perturbation during standing, while studying the offset of vibration will shed light on the post-effect of vibration on postural control. The purpose of this study was to investigate postural response in 6- and 10-year-old children while adapting to the altered visual and proprioceptive information during standing. We manipulated the proprioceptive information via tendon vibration and altered the visual information via vision occlusion. Because children at 6 and 10 years of age display an adult-like strategy to regulate variability but still show a higher magnitude of variability during quiet standing [23], we hypothesized that 6-year-old children may start showing an adultlike direction-specific postural response to unilateral Achilles tendon vibration, but the magnitude of response may not reach the adult level even in 10-year-old children.
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tendon. The outer casing of the motor was marked on the subject’s skin and checked periodically through the testing session to ensure the same placement. A pressure-sensing resistor (Interlink Electronics, Camarillo, CA) was placed between the Achilles tendon and the motor to provide an objective measure of pressure applied by the motor and helped standardize the attachment tension. Amplitude of vibration was found to dampen as much as 75 percent following tendon attachment to an individual [26]. Analysis of the pressure data from our first and last standing trials verified that each participant received the same stimulation applied by the motor across trials and groups. Participants stood barefoot on a Bertec 4060A force platform (Bertec, Columbus, OH) with their hands comfortably on the iliac crests. Kinetic data were collected by the force platform at a sampling rate of 600 Hz. Participants were instructed to maintain their normal standing posture while neither aligning their body rigidly nor swaying their body intentionally. The force platform was covered with a piece of brown butcher paper on which the feet were marked to ensure the same foot position throughout the data collection. Each standing trial lasted 40 s. The first 10 s were quiet standing without vibration and then vibration was triggered whenever the criterion was met. The criterion was that the force in the anterior–posterior (AP) axis was pointing to the anterior
[(Fig._1)TD$IG]
2. Methods 2.1. Participants Thirty healthy individuals participated in this study: younger children (YC, n = 10), older children (OC, n = 10), and young adults (YA, n = 10). Table 1 presents the physical characteristics of these participants. All the participants reported that they were free of any neuromuscular injuries or neurological disorders that would affect their ability in maintaining stable posture during standing. This study was approved by the Institutional Review Board at the University of Michigan. All the participants and the parents of the YC and OC groups gave written informed consent before participation. 2.2. Data collection A small wave pulse motor with an eccentric mass was used to stimulate the right Achilles tendon at 80 Hz [15,17,24,25]. The motor was measured 7 cm in length, 4 cm in width, and weighed 127.6 g. The motor was contained within a plastic cylinder with a concave surface to accommodate placement over the Achilles Table 1 Mean (SD) of the participant characteristics.
Gender Age (year) Body mass (kg) Height (cm) BOS_AP (cm) BOS_ML (cm)
YC
OC
5F/5M 6.33 (0.59) 20.80 (4.10) 114.10 (6.52) 18.56 (1.72) 24.96 (3.95)
6F/4M 10.33 (0.92) 35.30 (8.32) 137.05 (8.48) 21.46 (1.96) 25.10 (3.41)
YA 8F/2M 20.50 (1.39) 62.21 (11.01) 165.70 (8.86) 24.47 (1.60) 29.14 (2.75)
YC—younger children; OC—older children; YA—young adults; BOS—base of support; AP—anterior–posterior; ML—medial–lateral.
Fig. 1. A representative COP trajectory from a YA subject. The trajectory includes 5 s before the vibration onset (pre-vibration phase), 8 s of vibration (vibration phase), and 5 s after the vibration offset (post-vibration phase). Two vertical gray broken lines represent the vibration onset and offset, respectively. Timing of 0 s was the vibration onset and the vibration lasted for 8 s. (a) Anterior displacement was positive and posterior displacement was negative in the anterior–posterior (AP) direction. (b) Medial displacement was positive and lateral displacement was negative in the medial–lateral (ML) direction. The ML and AP directions were the xaxis and y-axis of the force platform, respectively.
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direction and the moment about the medial–lateral (ML) axis was causing an anterior rotation. The 8-s vibration was chosen to induce postural response in an optimal time window [19]. Two visual conditions were examined including eyes-open (EO) and eyes-closed (EC). In the EO condition, participants fixated a poster hung on the wall at their eye level about two meters away. In the EC condition, participants closed their eyes during each trial. Three 40-s trials were collected in each condition. The order of trials was randomized across the participants. Enough rest was provided between trials to minimize fatigue, particularly in younger children. Standing trials without tendon vibration were also collected and reported elsewhere [23]. 2.3. Data analysis Center of pressure (COP) data were analyzed in the AP and ML directions separately. Due to the differences in physical characteristics among three groups (such as base of support (BOS) in Table 1), COP data in the AP and ML directions were normalized to each participant’s BOS_AP and BOS_ML measures, respectively. Three phases of each standing trial were examined: 5 s before the vibration onset (pre-vibration phase), 8 s of vibration (vibration phase), and 5 s after the vibration offset (post-vibration phase). Average velocity was calculated as total excursion of the COP movement divided by the duration in each phase [27]. The Achilles tendon vibration at the right ankle induced the COP shifts in both the AP and ML directions. In the AP direction, the vibration onset induced a posterior COP shift and the vibration offset induced an anterior COP shift (Fig. 1a). In the ML direction, the vibration onset induced a medial COP shift and the vibration offset induced a lateral COP shift (Fig. 1b). The maximal COP shifts after the vibration onset and offset were considered to be the vulnerable positions which may cause a loss of balance. Therefore, the maximal posterior and medial COP shifts were examined after
[(Fig._2)TD$IG]
the vibration onset in the AP and ML directions, respectively, during the vibration phase. The maximal anterior and lateral COP shifts were examined after the vibration offset in the AP and ML directions, respectively, during the post-vibration phase. Timing of the maximal COP shift was determined as latency in seconds after the vibration onset during the vibration phase and latency in seconds after the vibration offset during the post-vibration phase. Mean COP position during the pre-vibration phase was used as the baseline when calculating the magnitude of the maximal COP shift. 2.4. Statistical analysis A series of 3 (Group) 2 (Visual) 3 (Phase) ANOVA with repeated measures on the last two factors were conducted on COP average velocity for all three phases in both the AP and ML directions. A series of 3 (Group) 2 (Visual) 2 (Phase) with repeated measures on the last two factors were conducted on the timing and magnitude of each maximal COP shift to compare the vibration and post-vibration phases. Absolute values of these magnitudes were used for this analysis while the original magnitudes were presented in Fig. 3. All the statistical analyses were performed using SAS software version 9.2 (SAS, Cary, NC). Significance level was set as p < 0.05. Post-hoc comparisons with Bonferroni adjustments were conducted when appropriate. 3. Results 3.1. COP average velocity In the AP direction, there was a group by phase interaction (p = 0.0219) and a visual by phase interaction (p = 0.0260) (Fig. 2a and c, Table 2). While all three groups increased average velocity from the pre-vibration phase to both vibration and post-vibration phases, both the YC and OC groups increased this variable to a greater extent than the YA group. The YC group produced a higher average velocity than the OC group, who produced a higher velocity than the YA group, during each phase. Compared to average velocity in the EO condition, the EC condition
Fig. 2. Mean and standard deviation of the COP average velocity. (a) In the EO condition and AP direction, (b) in the EO condition and ML direction, (c) in the EC condition and AP direction, and (d) in the EC condition and ML direction. Average velocity was normalized to the subjects’ base of support in the AP and ML directions, respectively. BOS_AP, base of support in the AP direction; BOS_ML, base of support in the ML direction; EO, eyes open; EC, eyes closed.
p = 0.2693 p = 0.9646 p = 0.5677 p = 0.6732 F(2,27) = 1.38, F(2,27) = 0.04, F(2,27) = 0.58, F(2,27) = 0.40, p = 0.6901 p = 0.8682 p = 0.9306 p = 0.5275 F(1,27) = 0.16, F(1,27) = 0.03, F(1,27) = 0.01, F(1,27) = 0.41,
F(1,27) = 51.30, p < 0.0001 F(1,27) = 13.08, p = 0.0012
F(1,27) = 1.58, p = 0.2195 F(1,27) = 15.64, p = 0.0005 F(1,27) = 1.07, p = 0.3098 F(1,27) = 4.33, p = 0.0472 F(2,27) = 2.19, p = 0.1315 F(2,27) = 36.38, p < 0.0001 F(2,27) = 2.31, p = 0.1187 F(2,27) = 11.31, p = 0.0003
Average velocity AP ML Maximal COP shift Timing: AP Magnitude: AP Timing: ML Magnitude: ML
F(2,27) = 43.28, p < 0.0001 F(2,27) = 23.05, p < 0.0001
p = 0.8705 p = 0.3677 p = 0.1218 p = 0.6096
F(2,27) = 3.10, F(2,27) = 5.00, F(2,27) = 0.59, F(2,27) = 4.04,
p = 0.0615 p = 0.0143 p = 0.5591 p = 0.0292 F(2,27) = 0.14, F(2,27) = 1.04, F(2,27) = 2.28, F(2,27) = 0.50, F(1,27) = 119.48, p < 0.0001 F(1,27) = 11.41, p = 0.0002 F(1,27) = 52.34, p < 0.0001 F(1,27) = 27.67, p < 0.0001
F(4,54) = 0.31, p = 0.8671 F(4,54) = 0.68, p = 0.6089 F(2,54) = 3.91, p = 0.0260 F(2,54) = 2.25, p = 0.1148 F(4,54) = 3.13, p = 0.0219 F(4,54) = 3.07, p = 0.0237 F(2,27) = 0.94, p = 0.4047 F(2,27) = 0.86, p = 0.4350 F(2,54) = 31.02, p < 0.0001 F(2,54) = 24.52, p < 0.0001
Group Visual Phase Group Phase Group
Table 2 Statistical results of the COP variables.
Visual
Phase
Group Visual
Visual Phase
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marginally increased average velocity during the pre-vibration phase, but significantly increased it during both vibration and post-vibration phases across all three groups. In the ML direction, there was a group by phase interaction (p = 0.0237) and a visual effect (p = 0.0012) (Fig. 2b and d, Table 2). Among the three phases of standing trials, both the YC and OC groups showed the greatest average velocity during the vibration phase and the smallest values during the pre-vibration phase. In contrast, the YA group had a similar average velocity across the three phases. The YC group produced a higher average velocity than the OC group, who produced a higher velocity than the YA group, during each phase. From the EO to the EC condition, all three groups increased average velocity. 3.2. Maximal COP shifts In the AP direction, there was a phase effect (p < 0.0001) on the timing of the maximal COP shift (Fig. 3a, Table 2). Across three groups and two visual conditions, mean timing of the maximal posterior shift during the vibration phase was 4.95 s after the vibration onset, and mean timing of the maximal anterior shift during the post-vibration phase was 2.85 s after the vibration offset. Also, there was a group by phase interaction (p = 0.0143) and a visual effect (p = 0.0005) on the magnitude of the maximal COP shift (Fig. 3b, Table 2). While the YC group had a similar magnitude between the vibration and post-vibration phases, both the OC and YA groups had a greater magnitude during the vibration phase than during the postvibration phase. The YC group had a greater magnitude than the OC and YA groups in both phases, whereas the OC group had a greater magnitude than the YA group only during the vibration phase. All three groups increased the magnitude of the maximal COP shifts from the EO to the EC condition during both vibration and postvibration phases. In the ML direction, there was a phase effect (p < 0.0001) on the timing of the maximal COP shift (Fig. 3c, Table 2). Across three groups and two visual conditions, mean timing of the maximal medial shift during the vibration phase was 4.50 s after the vibration onset, and mean timing of the maximal lateral shift during the postvibration phase was 2.88 s after the vibration offset. Also, there was a group by phase interaction (p = 0.0292) and a visual effect (p = 0.0472) on the magnitude of the maximal COP shift (Fig. 3d, Table 2). Both the YC and OC groups produced a greater magnitude during the vibration phase than during the post-vibration phase, whereas the YA group had a similar magnitude between the two phases. Both the YC and OC groups produced a greater magnitude than the YA group during the two phases. All three groups increased the magnitude of the maximal COP shifts from the EO to the EC condition during both vibration and post-vibration phases.
4. Discussion Both the YC and OC groups showed an adult-like directionspecific postural response to the Achilles tendon vibration above the right ankle during standing, i.e., a posterior COP shift in the AP direction and a medial shift in the ML direction after the onset of vibration, and an anterior COP shift in the AP direction and a lateral shift in the ML direction after the offset of vibration [16,19]. This finding suggests that children as young as 6 years of age develop an adult-like direction-specific postural strategy to respond to unilateral Achilles tendon vibration during standing. It implies that muscle spindles of gastrocnemius are sensitive to the Achilles tendon vibration in children as young as 6 years of age, and the increased discharge of these muscle spindles may induce the central nervous system to produce a directionally appropriate postural response. This finding is consistent with previous studies that children as young as 4 years show some adult-like somatosensory function during various standing tasks, but the maturation of the sensory systems continues until adolescence [7,8]. A greater COP average velocity in both the YC and OC groups suggests that regulation of postural sway velocity while adapting to unilateral tendon vibration may have not reached the adult level by 10 years of age. The OC group produced an adult-like response pattern in the AP direction such that the magnitude of the maximal COP shift was greater during the vibration phase than during the post-vibration phase. Further, the OC group displayed an adult-like magnitude of the maximal anterior COP shift during the postvibration phase in the AP direction. However, no adult-like response was observed from the OC group in the ML direction. These findings suggest that children at 10 years of age may not be able to concurrently regulate the COP movement in both the AP
[(Fig._3)TD$IG]
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Fig. 3. Mean and standard deviation of the timing and magnitude of the maximal COP shifts during the vibration and post-vibration phases. (a) Timing of the maximal posterior COP shift during vibration (in seconds after the vibration onset) and the maximal anterior COP shift during post-vibration (in seconds after the vibration offset) in the AP direction, (b) magnitude of the maximal posterior COP shift during vibration and the maximal anterior COP shift during post-vibration in the AP direction (posterior shift was negative and anterior shift was positive; normalized to the subjects’ BOS_AP measures), (c) timing of the maximal medial COP shift during vibration (in seconds after the vibration onset) and the maximal lateral COP shift during post-vibration (in seconds after the vibration offset) in the ML direction, and (d) magnitude of the maximal medial COP shift during vibration and the maximal lateral COP shift during post-vibration in the ML direction (medial shift was positive and lateral shift was negative; normalized to the subjects’ BOS_ML measures).
and ML directions while adapting to the right Achilles tendon vibration. Because a unilateral tendon vibration induces a greater COP shift in the AP direction than in the ML direction, children at 10 years of age may have to prioritize their response in the AP direction in order to avoid a loss of balance in this direction. This finding is consistent with our previous study in quiet standing such that children at both 6 and 10 years of age displayed an adult-like variability-partitioning strategy, but an adult-like magnitude of variability was not observed even in children at 10 years of age [23]. Taken together, we propose that there may be a two-phase postural development for both quiet and perturbed standing such that an adult-like direction-specific postural strategy develops first around 6 years of age and then a refinement process of magnitude regulation may continue beyond 10 years of age [5,28,29]. Both the YC and OC groups showed similar timings of the maximal COP shifts compared to the YA group, but only the OC group displayed an adult-like magnitude of the maximal anterior COP shift during the post-vibration phase in the AP direction while adapting to tendon vibration. This suggests that children as young as 6 years of age may have developed an adult-like temporal regulation of postural response, but an advanced spatial regulation may take more than 10 years to develop. This finding is consistent with the development of spatial and temporal parameters on pointing tasks in children at 7–10 years of age [30]. Previous studies also reported a similar temporal and spatial observation in EMG data such that children at 7–10 years of age show an adultlike EMG latency in gastrocnemius for a backward support surface translation and in tibialis anterior for a forward support surface translation, but may continue to develop the structural organization of muscle synergy between proximal and distal muscles as well as between agonist and antagonist muscles [1,6]. However, a
previous study using a backward support surface translation found that children at 7–10 years of age display adult-like spatial parameters such as peak COP amplitude and velocity, but not temporal parameters such as the timing of the COP peak [8]. Despite the inconsistent observations, all of previous studies suggest that control of spatial and temporal parameters for motor tasks may develop separately, which may involve distinct neural circuits and muscular systems and may be context dependent. Although the Achilles tendon vibration induces a backward postural sway just like a backward support surface translation, the integration of the sensory information may be different. While the Achilles tendon vibration mostly affects the spindle primary endings of gastrocnemius [11], a backward support surface translation may influence the plantar cutaneous information as well as other sensory messages from joint receptors and the vestibular system [1]. Given the inconsistent observations in spatial and temporal postural parameters in children, future studies, particularly with a longitudinal design, are warranted to reveal the time course of spatial and temporal development in various contexts of postural tasks. All three groups produced an anterior COP shift in the AP direction and a lateral shift in the ML direction after the offset of vibration, with respect to their mean COP position before the onset of vibration. This overcorrection response is consistent with the studies using a bilateral Achilles tendon vibration [16,20]. However, a previous study reported that bilateral Achilles tendon vibration induces both overcorrection and undercorrection responses, and the trunk orientation and pelvis tilt angle are different between these two responses [21]. Future studies are needed to investigate the orientation of body segments and leg muscle activation patterns in children while adapting to tendon
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vibration, which will help reveal the underlying kinematic and neuromuscular control strategies. Acknowledgments The authors are grateful to all the participants and their families for their participation in this study. Conflict of interest statement No author has any financial or personal relationship with other people or organizations that could inappropriately influence this work. References [1] Forssberg H, Nashner LM. Ontogenetic development of postural control in man: adaptation to altered support and visual conditions during stance. J Neurosci 1982;2:545–52. [2] Nashner L, Black F, Wall C. Adaptation to altered support and visual conditions during stance: patients with vestibular deficits. J Neurosci 1982;2:536–44. [3] Peterson ML, Christou E, Rosengren KS. Children achieve adult-like sensory integration during stance at 12-years-old. Gait Posture 2006;23:455–63. [4] Riach CL, Starkes JL. Velocity of center of pressure excursions as an indicator of postural control systems in children. Gait Posture 1994;2:167–72. [5] Schmid M, Conforto S, Lopez L, Renzi P, D’Alessio T. The development of postural strategies in children: a factorial design study. J NeuroEng Rehabil 2005;2:29. [6] Shumway-Cook A, Woollacott MH. The growth of stability: postural control from a developmental perspective. J Mot Behav 1985;17:131–47. [7] Hirabayashi SI, Iwasaki Y. Developmental perspective of sensory organization on postural control. Brain Dev 1995;17:111–3. [8] Peterka RJ, Black F. Age-related changes in human postural control: sensory organization tests. J Vestib Res 1990;1:73–85. [9] Eklund G. Position sense and state of contraction: the effects of vibration. J Neurol Neurosurg Psychiatry 1972;35:606–11. [10] Goodwin GM, McCloskey DI, Matthews PBC. Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science 1972;175:1382–4. [11] Roll JP, Vedel JP. Kinaesthtic role of muscle afferents in man, studied by tendon vibration and microneurography. Exp Brain Res 1982;47:177–90.
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