Developmental perspective of sensory organization on postural control

ELSEVIER

Brain & Development 1995; 17:111-3

Orginal article

Developmental perspective of sensory organization on postural control Shin-ichi Hirabayashi *, Yuuji Iwasaki Division of Neurology, Nagano Children'sHospital, Toyoshina 3100, Toyoshina-Machi, Nagano 399-82, Japan Received 6 October 1994; accepted 23 December 1994

The development of sensory organization on postural control was studied using computerized dynamic posturography. Generalized posturai stability increased with age but had not reached the adult level at the age of 15 years. The significance of each sensory component for postural control was analysed. Somatosensory function developed early and became comparable with the adult level at the age of 3 - 4 years. The visual function followed and reached the adult level at the age of 15 years. The vestibular function developed later, showing a considerably lower level even at the age of 15 years. Girls were superior to boys with respect to the vestibular function at the age of 7 - 8 years. The implication of this sexual difference for some developmental disorders is discussed. Keywords: P o s t u r a l control; S e n s o r y o r g a n i z a t i o n ; D y n a m i c p o s t u r o g r a p h y ; V e s t i b u l a r f u n c t i o n

1. I N T R O D U C T I O N Multimodal sensory systems, including the visual, somatosensory and vestibular ones, are involved in maintaining the postural balance. In adults, they are well organized and act in a context-specific manner [1]. In children, however, how these sensory systems become organized with age remains uncertain. In order to clarify the developmental aspects of sensory organizatic~n on postural control, we examined the postural control of normal children under various sensory conditions using dynamic computerized posturography.

2. S U B J E C T S A N D M E T H O D S Ten children, 5 boys and 5 girls, of each age group from the first grade of kindergarten (3 or 4 years of age) to the third grade of junior high school (14 or 15 years of age)were recruited for this study with family consent. After excluding children with mild developmental disabilities, such as excessive clumsiness, an attention-deficit or poor academic achievement, 112 children (:56 boys and 56 girls) finally entered the study. Twelve children (5 boys and 7 girls) aged 3 - 4

* Corresponding author. Fax: (81) (263) 73-5432. 0387-7604/95/$09.50 © 1995 E][sevierScience B.V. All rights reserved SSDI 0387-7604(95)00009-7

years, 21 (11 boys and 10 girls) aged 5 - 6 years, 18 (9 boys and 9 girls) aged 7-8 years, 22 (11 boys and 11 girls) aged 9-10 years, 20 (10 boys and 10 girls) aged 11-13 years, and 19 (10 boys and 9 girls) aged 14-15 years were examined. Twenty-six adults over 20 and under 60 years of age (15 males and 11 females) were also examined. The EquiTest System (NeuroCom International Inc.) was used in this study. The equilibrium score indicating postural stability compared the subject's sway to the theoretical limits of stability. The subject's sway was calculated from the maximum anterior and posterior COG (center of gravity) displacements occuring over the 20-s trial period. The theoretical maximum displacement without losing balance was assumed to be a range of 12.5 ° (6.25 anterior, 6.25 posterior) [2]. The results were expressed as percentages, 0 indicating sway exceeding the limit of stability and 100 indicating perfect stability. The equilibrium score was examined under 6 different sensory conditions. Under condition 1, when the patient stood on a fixed platform with the eyes open, all three sensory systems were operational and a baseline measure of stability was obtained. Condition 2 was the same as condition 1 except that the patient had the eyes closed. Under condition 3, the patient was in the same position as for condition 1 but the visual surround moved to track h i s / h e r sway, which provided orientationally inaccurate visual cues. Under condition 4, the patient stood with the eyes open and the visual surround fixed but the platform moved in response to h i s / h e r

112

S.-L Hirabayashi, Y. Iwasaki / Brain & Development 1995; 17:111-3

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Fig. 1. Development of each sensory function contributing to postural control. For the definition of each function, see text.

sway so that the ankle joints did not bend in response to the sway, which provided inaccurate proprioceptive input to the brain. Condition 5 was identical to condition 4 except that the eyes were now closed, such that only the vestibular system was fully operational. Condition 6 was the same as condition 4 except that the visual surround moved in response to the patient's sway, and thus both vision and proprioception were compromised and only the vestibular system could be relied upon. Each condition was repeated three times except for conditions 1 and 2. The average score for all 6 conditions was taken as indicating the composite ability of sensory organization. In order to identify the significance of each sensory system influencing postural control, the ratios of condition 2 / c o n d i t i o n 1, condition 4 / c o n d i t i o n 1 and condition 5 / c o n dition 1 were interpreted as reflecting the somatosensory, visual and vestibular functions, respectively. The sex difference for each condition and ratio was also examined. Statistical differences between age groups were tested using A N O V A , and to identify the statistical difference between two neighboring groups the t-test was used.

age groups, significant differences were observed between the score at age 7 - 8 and that at age 9-10, between that at age 14-15 and that of adults in condition 5, and also between the score at age 9 - 1 0 and that at age 11-13 in condition 6 ( P < 0.05). The composite score showed a significant difference between the age 9 - 1 0 group and the 11-13 one, and also between the age 14-15 one and the adults ( P < 0.05). Each sensory function defined in section 2 is shown in Fig. 1. The children aged 3 - 4 had almost the same somatosensory function as the adults. Concerning the visual function, significant differences were disclosed between the age 5 - 6 group and the 7 - 8 one, and between the age 11-13 and age 14-15 ones ( P < 0.05). The vestibular function showed significant differences between the age 7 - 8 group and the 9 - 1 0 one, and also between the age 14-15 one and the adults ( P < 0.05). The children aged 7 - 8 showed significant differences between boys and girls with respect to condition 5 and also the vestibular function ( P < 0.05). That is, girls aged 7 - 8 were significantly superior to boys of the same age in the use of the vestibular cues under the condition of no visual cues and inaccurate somatosensory input (Fig. 2).

4. D I S C U S S I O N 3. R E S U L T S The equilibrium scores in each age group are shown in Table 1. All the conditions and composites exhibited significant differences between ages. O n comparing neighbouring

Posturai control requires two distinct processes [3]. O n e is the sensory organizational process, in which one or more of the orientational senses (visual, somatosensory and vestibular) are involved and integrated within the CNS. The other is

Table 1 Equilibrium scores: mean (standard deviation) Condition

3-4 years n = 12

5-6 years n = 21

7-8 years n = 18

9-10 years n = 22

11-13 years n = 20

14-15 years n = 19

20-59 years n = 26

1 2 3 4 5 6 Composite

76.7 (8.4) 74.6 (5.7) 65.2 (14.1) 44.3 (17.5) 29.0 (16.0) 24.5 (14.1) 45.4 (12.2)

83.3 (8.6) 77.9 (9.8) 74.6 (10.0) 56.0 (13.1) 33.2 (14.9) 28.6 (13.7) 52.7 (9.9)

86.8 (3.9) 82.8 (6.8) 81.9 (5.2) 63.6 (12.0) 33.3 (15.2) 36.2 (15.3) 58.2 (8.2)

88.7 (4.3) 85.5 (4.9) 85.0 (5.2) 65.3 (10.6) 44.1 (11.4) 34.2 (16.7) 61.3 (7.1)

91.5 (3.0) 90.1 (2.7) 88.8 (4.0) 71.9 (12.0) 48.7 (16.4) 48.6 (15.4) 68.1 (7.3)

91.8 (2.8) 90.4 (2.2) 88.2 (3.0) 78.0 (6.4) 49.4 (12.6) 49.4 (11.9) 70.0 (5.0)

93.2 (1.7) 91.0 (3.6) 87.7 (4.7) 83.2 (11.1) 63.5 (10.6) 59.0 (14.7) 75.7 (7.2)

S.-I. Hirabayashi, Y. lwasaki ~Brain & Development 1995; 17:111-3

the motor adjustment process, involved in executing coordinated and properly scale6 musculoskeletal responses. It is said that the motor process is an automatic, hierarchically lower process that develops in early childhood, whereas the sensory process is hierarchically higher and develops more slowly [4]. The sensory organizational process in adults is contextspecific [1]. In a well-practised situation, like standing on a stable surface, somatosensory input plays the primary role in maintaining balance, visual input being rather auxiliary. On the other hand, visual input is important in a novel situation or a situation where the support surface is unstable. The vestibular system acts as a referential function and is critical in resolving inter-sensory conflict by suppressing input not congruent with vestibular input. With the EquiTest system, conditions 1, 2 and 3 provide situations in which somatosensory input plays the primary role in postural control. Condition 4 provides a situation where the support surface is unstable and visual input is important. Conditions 5 and 6 comprise artificial situations in which the vestibular system should act as a reference for managing the inter-sensory conflict. Our study confirmed the marked developmental change with respect to the sensory organization on postural control. Even condition 1 revealed a developmental change, in that the preschoolers showed considerably lower scores compared with the adults. This is considered to reflect the immaturity of the basic neuro-muscular mechanism involving both the sensory and motor processes responsible for the postural control at preschool age. The children aged 3 - 4 years showed levels of somatosensory function equivalent to the adults. The visual function developed more slowly and the children aged 14-15 years had the same level as the adults. The vestibular function developed more slowly than the visual function. Even at the age of 14-15 years it had not reached the adult level. This showed that the referential function of the vestibular system developed more slowly than the primary functions of the other two sensory systems. Shumway-Cook et al. suggested that with development there was a shift in the dominant sensory inputs on postural control, but at the age of 7-10 years the response patterns became comparable to that in adults, suggesting that by this age maturation of organizational processes required to integrate sensory inputs had occurred [1]. Forssburg and Nashner showed that young children below the age of 7.5 years were unable to systematically suppress the influence of inputs derived from the support surface or from vision when they provided inappropriate ori,:ntational information [4]. Our results, however, showed that such a maturational process occurred more slowly than expected from previous studies, and continued throughout childhood but had not reached the adult level even at the age of 14-15 years.

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Another interesting finding in our study was a clear female predominance with regard to the vestibular function at the age of 7-8 years. Riach and Hayes also noted that boys younger than 10 years swayed substantially more than girls of the same age, suggesting a greater level of postural instability in boys of that age [5]. These facts conform to the clinical impression that young boys in lower grades at primary school are prone to being more clumsy with respect to motor coordination than girls of the same age. Ayres revealed the significance of sensory integration, in which the vestibular function was considered to play a critical role, not only for motor adjustment but also for higher cerebral functions like attention control or cognition essential for learning [6]. Using the same method as that applied in this study, Horak et al. demonstrated sensory organizational deficits in learning-disabled children [7]. It is possible that the maturational slowness of the vestibular function seen in young boys is one of the factors responsible for the fact that boys are prone to be more attentive and hyperactive than girls, and that the attention deficit-hyperactivity disorder (ADHD) and learning disabilities (LD) exhibit a definite male preponderance. The EquiTest system seems the more useful tool for detecting a subtle equilibrium dysfunction, compared with conventional vestibular function tests. It is also expected to be useful for monitoring functional disorders of CNS origin related to posture or balance, such as the developmental coordination disorder frequently co-existing with A D H D or LD. This study provides normative data for comparison with data for such disorders.

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