The goal of this study was to assess the development of postural regulation in typically developing children reflected by their postural reactivity to dynamic, virtual visual environments. The first important finding is that for the youngest group (5- to 7-year-olds) visual input was disproportionately influential compared to proprioceptive and vestibular inputs on postural regulation. This was reflected by the qualitative finding that most participants in this age group were not able to complete the dynamic trials. Regarding the other age groups, body sway to different frequencies decreased significantly with age up until 16–19 years. Similarly, vRMS decreased significantly with age before reaching adult levels at around 16–19 years of age. These results are interpreted as suggesting an important transitory period regarding the maturation of the systems underlying sensorimotor integration at around 16 years of age.
As was mentioned earlier, oscillation frequency had a significant effect on BS, given that across age groups, the largest amount of sway was found for the 0.25-Hz condition. This is consistent with Sparto et al.'s (
2006) findings where a peak in postural sway was observed at 0.25 Hz for 7- to 12-year-old children, suggesting that the use of dynamic cues for postural control is frequency dependent. Other studies have shown that the coupling of sway to optic flow was more important in the 0.2- to 0.3-Hz range; in other terms, 0.25 Hz could be a more natural speed of environmental movement, which makes it a frequency of choice for inducing sway (Dijkstra, Schöner, Giese, & Gielen,
1994; Giese, Dijkstra, Schnoer, & Gielen,
1996; Schöner,
1991).
The BS of the adult group at 0.5 Hz was clearly lower compared to the BS for the two other frequencies. This is in agreement with evidence from Stoffregen (
1986) who found that when exposing adults to an oscillating room, a weaker correlation was observed between room movement and postural sway at higher frequencies compared to lower frequencies (frequency range: 0.2–0.8 Hz). Similarly, van Asten, Gielen, and van der Gon (
1988) found that when adults were exposed to a rotating display above a 0.3-Hz frequency, compensatory lateral sway did not occur. In addition, when exposed to frequencies higher than 0.3 Hz, postural sway equaled that observed when participants had their eyes closed. In contrast to adults, infants and young children seem to use both high and low frequencies for postural control. Delorme, Frigon, and Lagacé (
1989) found that 7- to 48-month-old infants that were exposed to an oscillating swinging room responded to a frequency as high as 0.52 Hz, as illustrated by the synchronicity of their postural sway with the room's oscillation frequency. Similarly, Bai (
1991) found that infants aged between 5 and 13 months exposed to an oscillating room responded to frequencies in the 0.3-Hz to 0.6-Hz range. Finally, Schmuckler (
1997) found that children between the ages of 3–6 years reacted to a range of 0.2–0.8 Hz swinging room oscillation frequencies but adults did not.
Similar to the BS findings, results from the present study clearly demonstrate a significant decrease in vRMS (or increase in stability) with age. For the 8- to 15-year-old group, there was an effect of frequency where the greatest instability was induced by the 0.5-Hz frequency, followed respectively by 0.25 Hz and 0.125 Hz. However, a frequency effect was not observed for the 16- to 19-year age groups. In addition, when averaged across frequency, mean vRMS for the 16- to 19-year-old group was adult-like, that is, it did not significantly differ from that of the 20- to 25-year-old group.
This finding is in accordance with previous data from Steindl, Kunz, Schrott-Fischer, and Scholtz (
2006) who showed that the visual afferent system reached an adult level at 15 to 16 years of age with regards to the maintenance of postural balance (see also Aust,
1991; Hirabayashi & Iwasaki,
1995). Largo, Fischer, and Rousson (
2003) found that static balance, as assessed by the Zurich Neuromotor Assessment continued developing until 18 years of age. Other studies have found that optimal stance stability is reached by the age of 15 years old (Cherng, Chen, & Su,
2001; Hirabayashi & Iwasaki,
1995; Peterka & Black,
1990).
A possible explanation for the decrease in BS at 0.5 Hz for the older versus the younger groups in our data could be inertia of the body that may differ for the older groups resulting in greater difficulty swaying at these higher frequencies. This may help explain why 0.5-Hz sway was greater than 0.125-Hz sway in the younger children but not the older. Although this is an interesting possibility, we do not believe that inertia is driving this difference. The reason is that we have recently conducted some measures across life span (Greffou & Faubert,
2008) and found that older adults, who presumably have similar inertia as the young adults, have responses identical to the younger observers in the present study for the 0.5-Hz condition. That is, the 0.5-Hz BS was greater in the older observers than the young adults and therefore cannot be the result of differences in body inertia.
In the following sections, the present findings will be discussed within the context of existing frameworks implicating different regulatory systems involved in visuo-motor integration as a function of age. Five different frameworks will be addressed:
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visuo-motor brain processing that underlies postural regulation reaches adult levels at around 16 years of age;
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children rely more heavily on visual information to regulate their posture due to their immature vestibular and somatosensory systems;
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children have greater difficulty dealing with conflicting sensory information, hence exhibiting postural instability;
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the habituation phenomenon, which is a gain in experience in the control of posture; and finally
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Woollacott and Shumway-Cook's (
1990) systems theory of development where children progressively acquire systems that allow them to control posture.
Visuo-motor processing that underlies postural regulation requires the activation of many brain areas. A study by Slobounov et al. (
2006) has looked at the neural underpinning of postural responses to visual field motion using virtual reality stimuli. They found significant activation of motion sensitive areas V5/MT (Middle Temporal area) and STS (Superior Temporal Sulcus), suggesting that the brain has an extensive but unified visual motion processing system (this finding was true for an anterior–posterior virtual room displacement stimulus at 0.3 Hz). They also observed the activation of prefrontal and parietal areas bilaterally which they believed was due to fronto-parietal network for attentional modulations; this finding is consistent with those of Friston, Holmes, Poline, Price, and Frith (
1996) who suggested a supra-modal role of the prefrontal cortex in attention operating both in the mnemonic and sensorimotor domains. Slobounov et al. (
2006) suggest that there is a functional interaction between modality specific posterior-visual and frontal–parietal areas that subserve visual attention and other perceptual-motor tasks. Moreover, the bilateral activation of the parietal cortex can be explained by the fact that parietal systems play an important role in the perception and the analysis of complex motion patterns and in the control of planned action. They observed a bilateral activation of the cerebellum during the presentation of a moving virtual room; the cerebellum is involved in the execution of motor tasks but also in the cognitive task of judgment of motor activity and in the timing system providing precise temporal representation across motor tasks. Finally the ACC (Anterior Cingulate Cortex) was activated, which is thought to be responsible for attentional control. As demonstrated above, there are many brain areas solicited for postural control. It is quite probable, therefore, that the integration of these brain systems would take some time to mature and our data suggest that this would occur at the earliest around 16 to 19 years of age.
Some have argued that children rely more heavily on visual cues than adults to control their posture due to their inability to use the vestibular and somatosensory information available (Forssberg & Nashner,
1982; Shumway-Cook & Woollacott,
1985). It nonetheless appears, in the light of our findings, that the effects of age and of oscillation frequency on instability are contingent on
dynamic visual input information and not on immature vestibular motor systems. If the vestibular and somatosensory systems were immature in children, we would have observed a difference in instability even in the presence of a static environment (static tunnel), which was not supported by our data. Peterka and Black (
1990) also demonstrated that instability for children was no different from that of adults when exposed to a static environment.
An existing theory proposes that children rely more heavily on visual input to regulate their posture compared to adults because they have difficulty dealing with conflicting sensory information (Barela, Jeka, & Clark,
2003; Forssberg & Nashner,
1982; Shumway-Cook & Woollacott,
1985). Forssberg and Nashner (
1982) have suggested that children below the age of 7.5 years are unable to reweigh multiple sensory inputs, which is congruent with the qualitative results demonstrating that children below 8 years of age were unable to complete the dynamic trials. In contrast, the Bair, Kiemel, Jeka, and Clark (
2007) study assessing somatosensory vs. visual inputs reweighing in children aged 4 to 10 years has shown that children can reweigh multisensory inputs from 4 years on. However, the amount of reweighing increased with age and reweighing contributed to a more stable and flexible control of upright stance. Along these lines, a possible explanation for the observed stability plateau in the present study could be that around 16 years of age, children become very competent at dealing with conflicting sensory information or at reweighing the different sensory afferences (e.g., when proprioceptive and vestibular inputs remain unchanged while the visual input is altered).
The fact that we did not observe an effect of frequency on vRMS in participants whose ages were 16 years onward could potentially be explained by the “Habituation” phenomenon. This phenomenon was addressed by Schmuckler (
1997) who found that in later trials, body sway to dynamic visual stimuli was significantly decreased when compared to identical earlier trials for the same participant. Hence, it may be possible to generalize this phenomenon to everyday experiences, in that, older teenagers and adults may have habituated to dynamic environments to which they have been exposed for a longer period than the younger children therefore reacting less.
Among the different developmental theories on postural control lies Woollacott and Shumway-Cook's (
1990) who have argued in favor of two different explanations:
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The “strict vertical hierarchy hypothesis,” which claims that infants first use a cephalocaudal gradient and a primitive reflex system in establishing stability but develop more mature higher nervous system centers (in the cortex) that take over the function of postural control; and
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the “Systems Theory,” where the development of independent stance emerges from the interaction among multiple neural and biomechanical components.
These components are the following: postural muscle response synergies; visual, vestibular, and somatosensory systems for detecting loss of balance; adaptive systems for modifying sensory and motor systems to changes in task; muscle strength; joint range of motion; and body morphology. According to this hypothesis, transitory phases of development would occur whenever one or many of the components mature. A possible explanation for our study's findings would be that all of these components may finish maturing around 16 to 19 years of age and that important ones become developed after 8 years of age as reflected by a higher stability and a lower postural reactivity of children between 8 and 15 years old compared to the children of 5 to 7 years old. Similar findings were reported by Shumway-Cooke and Woollacott (
1985) who observed that the onset and timing of the response of 4- to 6-year-old children to platform perturbations were markedly different from that of older children. During development of postural control, there are musculoskeletal and body morphology changes such as height, center of mass, and foot length. Depending on the combination of these different components, a person will choose either of these three strategies:
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the ankle strategy in which balance adjustments are made at the ankle joint,
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the hip strategy where adjustments are made at the hip, and
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the suspensory strategy in which the person flexes at the knee, ankle, and hip to lower the center of gravity toward the base of support.
As children's heights change with the passage of time, resulting musculoskeletal changes influence their stability but also the type of strategy that will be chosen to achieve stability. In the light of our study, perhaps musculoskeletal development achieves adult levels around 16–19 years of age.
Finally, different muscle synergies are exhibited during balance control depending on age. For example, Sundermier, Woollacott, Roncesvalles, and Jensen (
2001) found that children between the ages of 4–10 years used different muscle synergies than the younger children who were 1 and 2 years old. Changes in muscle synergies probably continue to develop above the age of 10 years and could possibly account for the differences observed in our study.