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Peripheral vision and age-related differences in dynamic balance
Human Movement North-Holland
Science
533
11 (1992) 533-548
Peripheral vision and age-related differences in dynamic balance C. Assaiante Laboratoire
and B. Amblard
de Neurosciences
*
Fonctionnelles,
CNRS, Marseille, France
Abstract
Assaiante, C. and B. Amblard, 1992. Peripheral balance. Human Movement Science 11, 533-548.
vision and age-related
differences
in dynamic
The purpose of this study was to investigate the role of peripheral visual cues in locomotor equilibrium as a function of age in 3- to 12.year-old children and adults. Peripheral visual restrictions (PVR), limiting frontal vision to either 30, 60 or 120 degrees, were applied to subjects walking on a narrow beam. The subjects’ locomotor equilibrium performances were evaluated in terms of the locomotor speed, which constitutes a good index to the difficulty of locomotor balancing. The results showed that the influence of peripheral visual cues on locomotor equilibrium control did not vary monotonously with age. The peripheral visual contribution to dynamic balance control increased from 3 to 6 years of age, with a maximum in h-year-old children. The peripheral visual influence on locomotor equilibrium control then disappeared suddenly in the 7-year-old children. It tended to increase again from 8-9 years of age to adulthood. In adults, the peripheral visual contribution to locomotor equilibrium that we have described previously was confirmed and compared to that involved in postural control. It is concluded from these results that late improvements occur in locomotor balance control during childhood.
Introduction Peripheral visual cues as well as motion visual cues have been reported to play a particularly important role in the control of postural (Amblard and Carblanc 1980; Paulus et al. 1984; Amblard et * We are grateful to Bernard Assaiante revising the English. Correspondence to: C. Assaiante, UPR 13402 Marseille-Ctdex 9, France.
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al. 1985; Stoffregen 1985) as well as locomotor equilibrium in adults (Assaiante et al. 1989; Assaiante 1990). Some studies on babies (Jouen 1986) and young children (Lee and Aronson 1974; Brandt et al. 1976; Butter-worth and Hicks 1977; Stoffregen et al. 1987) have also indicated that visual, particularly peripheral cues, play a prominent role in the elaboration and control of static postural equilibrium. It has been reported moreover that vision predominates in infants during transitional periods in which they attempt to master new postural challenges (Butterworth 1986). It has been observed that the sensitivity to visual flow increases as the infants learn to sit without support (Butterworth and Hicks 1977). This sensitivity increases again with the onset of upright stance (Lee and Aronson 1974) and with the onset of unaided walking (Stoffregen et al. 1987). These transition phases are not restricted to babyhood, however. Recent studies (Shumway-Cook and Woollacott 1985) have shown that a transition phase in postural development occurs in 4- to 6-year-old children, which suggests that postural control improvements continue to take place during childhood and that some changes with age in the use of visual cues can probably be observed. Up to now, developmental studies have focused particularly on the visual contribution to static postural equilibrium, but very little attention has been paid to the changes in the use of visual cues in locomotor equilibrium control as a function of age. Owen and Lee (1986) have reported that 3- to 5-year-old walkers showed body oscillations in response to an optical flow, artificially induced with a moving room. Stoffregen et al. (1987) also reported that in young walkers (up to 5 years of age) an optical flow, artificially induced with a moving room and presented only to the periphery of the visual field, resulted in a higher level of compensatory postural responses than when centrally presented. According to these authors, this difference resulted from the dynamic geometrical structure of the optical flow normally associated with locomotion. This structure is radial in the center of the optical flow and lamellar in its periphery. Stoffregen et al. concluded that children in the age range 2-5 years show the same relative sensitivity as adults to the dynamic structure of the peripheral optic array in controlling posture. The main purpose of the present study was to examine the developmental changes in the use made of peripheral visual cues from the natural optical flow associated with locomotion in controlling balance
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during walking, in 3- to 12-year-old children. In order to specifically test the lateral equilibrium component of locomotion, we asked our young subjects to walk on a narrow beam. We have previously reported that this locomotor task actually produced an enhancement of the body sway in the frontal plane, attesting to an increase in the level of lateral equilibrium difficulty (Assaiante 1990). In order to evaluate the contribution of visual factors to balance control while walking on a narrow beam, we subjected the subjects to peripheral visual cue restrictions. The peripheral visual field was variably restricted by means of appropriate spectables limiting vision to the frontal field (Assaiante et al. 19881. The subjects’ performances were evaluated by simply measuring the locomotor speed on narrow supports, which has been previously shown to be highly sensitive to the supplementary difficulty of maintaining dynamic lateral equilibrium encountered under restricted visual conditions, in both animals (Marchand and Amblard 1984, 1990) and humans (Assaiante et al. 1989).
Methods Subjects Two hundred and fifteen normal healthy children from 3 to 12 years of age participated in this experiment. The youngest were recruited from a nursery school and the others from a primary school. Ten groups of subjects were formed on the basis of their age (for example, ‘age 3’ contained 2.5 to 3.5year-old children). From youngest to oldest, these ten age groups consisted of twenty-four, twenty-nine, twenty-four, thirty-two, twenty-three, twenty-three, twenty-five, twenty-two, eight and five children, respectively. The same groups included fifteen, nineteen, nine, fifteen, twelve, fifteen, thirteen, twelve, three and four males, respectively. A control group consisting of twelve healthy adults, five women and seven men aged from 20 to 45 years underwent the same experiment. Tasks and surroundings The experiment was performed in a primary school gymnasium (30 m wide, 45 m in length) providing the children with a familiar
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environment. Locomotor equilibrium was studied on a narrow support (wooden beam, 10 cm wide, 20 cm high, 6 m long). The locomotor speed was measured by means of an infrared optical device and an electronic timer, over a distance of 5 m excluding the first 50 and the last 50 cm of the total beam length to eliminate the initial acceleration and final deceleration. The infrared optical device did not involve any cable being attached to the subjects, who were totally free to walk on the beam. The subjects had to walk as fast as possible on the beam. When the subjects lost balance during a trial, they were requested to perform another trial until they succeeded under the same experimental conditions. These falls were independent of the visual conditions and almost were no longer observed from 4-5 years of age onwards.
Visual conditions Peripheral visual restrictions (PVR) were applied by means of appropriate spectacles. The neutral glasses of these spectacles were partly covered with black adhesive tape, in such a way that vision was possible only through a central vertical slit in front of each eye. The widths of these slits were chosen so as to obtain binocular central visual fields of either 30, 60, or 120 degrees. Complementary black protective devices were used around the frames of the spectacles to avoid undesirable lateral vision. Whatever the PVR, the locomotor support always remained visible in front of the subject. Moreover, two control situations were included: normal vision (NV) (without spectacles) and vision through neutral spectacles (NS) without any other visual limitations.
Experimental session Either four to six children or two adults were tested at each session. Under a given visual condition, they performed the task in turn so that each was able to rest between his own successive trials. With each visual condition, the locomotor task was run twice according to a pseudo-random plan, and the results of the two trials performed by each subject were averaged.
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Analysis The speed values were converted into logarithms and the results obtained with all the subjects in each age group were pooled for the graphs. A log scale was preferred to a linear scale in the figures because it shows up the relative rather than the absolute changes in speed depending on the visual conditions, and therefore yields comparable dispersions over a wide range of absolute speeds (Marchand and Amblard 1984, 1990; Assaiante et al. 1989). The log transform of speed was also used for the statistics because the comparisons involved a wide range of absolute speeds, with some of the values approaching the lower limit (zero speed). In view of the variations in the number of subjects from one group to another, an appropriate ANOVA program VAR3 ’ was used to test the degree of significance of the comparisons made between experimental situations. A regression analysis was also carried out to test the changes with age in the locomotor speed under normal vision. Lastly, with each age group and visual condition, the relative loss of speed (see below) was used in a one-sample analysis (t-statistic) against the null hypothesis (STATGRAPHICS program).
Results The individual locomotor speeds while walking on a narrow beam under normal vision (fig. l), in 3- to 12-year-old children and in adults, were subjected to a regression analysis. It can be seen from this figure that the mean speed increased quite regularly with age in the 3- to 9-year-old children with a fairly sharp slope (0.285 + 0.010, with t = 26.11); whereas it almost reached a plateau from the age of 9 up to adulthood, as attested by the very gentle slope (0.012 f 0.008, with t = 1.45). Moreover, the individual variations in locomotor speed under normal vision did not show any clearly detectable changes with age, as attested in fig. 1 by the roughly constant dispersion. The average locomotor speed while walking on a narrow beam under various visual conditions is shown in log scale in fig. 2, in 3- to ’ Rouanet, report.
P., M.O.
Lebeaux
and
D. Ltpine,
Programme
VAR3,
Univ.
of Paris
6, Internal
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I
I
I
I
J
I
I
I
I
e
5
10
15
20
1 a5
AGE(years) Fig. 1. Individual locomotor speed while walking on a narrow beam under normal vision as a function of age. The two straight lines result from linear regression analyses of speed versus age in the 3- to 9-year-old (left side) and Y-year-old to adult age groups (right side).
12-year-old children and in adults. The mean locomotor speed was highly dependent upon the subjects’ age (F(8, 16.5) = 38.9, p < 0.001) under all the visual conditions. Within a given age group, the effects of the visual factor (5 visual conditions) were significant in all the age groups, except in the 12-year-old children (see details in table 1). These results confirmed that peripheral vision is used to control lateral dynamic equilibrium in childhood, at least while walking on a narrow support. The curves in fig. 2, which are roughly parallel, suggest that peripheral visual restrictions induced relative rather than absolute changes in the locomotor speed. It can be seen moreover from fig. 2 that these relative changes in speed depending on the visual conditions differed among the
C. Assaiante, B. Amblard / Peripheral uision and dynamic balance
1 30
I
I
1
4
60
vm
ws
NV
Fig. 2. Mean locomotor speed on narrow beam as function of age (in years; ad: adults) conditions: frontal vision limited to 30, 60 or 120 degrees; neutral spectacles without field limitation (NS); normal vision without spectacles (NV).
539
and visual any visual
various age groups studied, which indicates that the way in which PVR influenced the locomotor speed depended upon the subjects’ age. In order to specify this effect, we have calculated the ‘relative speed’ RS, obtained under each PVRi condition (i = 30, 60 or 120) by comparing the absolute speed (Si> (but not its log transform) obtained under PVRi with the speed (S,,) obtained with neutral spectacles: RS, = 100 - (S,,
- S,)/S,,
= 100 - RLS,,
where RLSi was the ‘relative loss of speed’ due to PVR,. The latter visual condition S,, was chosen as a control situation in order to
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Table 1 Significance levels determined by applying ANOVA to the visual effects on the locomotor speed (second column) and by performing one-sample analysis (t-statistic) to the relative loss of speed in the case of frontal vision limited to 30 degrees (third column). Age group 3 years 4 years 5 years 6 years 7 years 8 years 9 years 10 years 11 years 12 years Adults
Visual effects
RLS,n
F(4,92) = 8.98 p < 0.001 F(4.112) = 6.39 p < 0.001 F(4.92) = 7.30 p < 0.001 F(4,124)= 15.42 p < 0.001 F(4,88) = 4.96 p < 0.01 F(4.88) = 3.14 p < 0.05 F(4.96) = 16.03 p < 0.001 F(4,84) = 5.91 p < 0.001 F(4,28) = 8.76 p < 0.001
t(23) = 2.63 p < 0.05 t(28) = 2.21 p < 0.05
tl.S.
F(4,44) = 4.97 p < 0.01
“.S.
t(31) = 6.96 p < 0.001 n.s. “.S.
t(24) = 2.96 p < 0.01 “.S. t(7) = 2.98 p < 0.05 n.s. t(11)= 3.83 p < 0.01
avoid the artefacts induced by spectable wearing in children who are not accustomed to wearing spectacles. We often observed significant differences in mean locomotor speed between normal vision (NV) and neutral spectacle (NS) conditions, as can be seen from table 2. There seems to be no obvious explanation for this phenomenon. The relative speed corresponding to each of the three PVR conditions is presented in fig. 3 as a function of the subjects’ age. The severest visual restriction naturally induced the greatest loss of speed in comparison with the normal spectacle-wearing conditions. The relative loss of speed due to frontal vision being limited to 30 degrees was significant in most of the age groups (see details in table 1). RLS,, was maximum in 6-year-old children: the relative speed RS,, was in fact lower in the 6-year-olds than in the 5-year-olds (F(1.54) = 4.4, p < 0.05), and was also lower in the 6-year-olds than in the 7-year-olds (F(1,53) = 10.9, p < 0.01). Moreover, little difference in speed was
C. Assaiante. B. Amblard / Peripheral rision and dynamic balance Table
541
2
Significance levels determined by applying between neutral spectacles (NS) and normal Age group
3 years 4 years 5 years 6 years 7 years 8 years 9 years 10 years 11 years 12 years Adults
ANOVA to the differences visual (NV) conditions.
in locomotor
speed
Difference between NS and NV conditions F(1,23) = 7.07 p < 0.05 F(1,28) = 4.49 p < 0.05 F(1,23) = 7.88 p < 0.01 n.s. F(1,22) = 4.30 p < 0.05 F(1,22) = 7.94 p < 0.01 F(1,24) = 14.03 p < 0.001 F(1,21) = 4.32 p < 0.05 F&7) = 12.25 p < 0.01 n.s. n.s.
observed between the 30 degrees and neutral spectacles conditions in the 7-year-old subjects, but thereafter this difference tended to increase with age (p < 0.07) up to adulthood, when this difference becomes very significant (see details in table 1). The latter result confirmed the importance of peripheral vision in controlling locomotor equilibrium in adults (Assaiante et al. 1989). Considerable similarity exists between the three curves in fig, 3 from 4 years of age to adulthood. Indeed, in the case of frontal vision limited to 60 degrees, significant differences in RS,, were again observed both between 5 and 6 years of age (F(1,54) = 4.95, p < 0.05) and between 6 and 7 years of age (F(1,53) = 12.20, p < 0.001). The RS difference between 6 and 7 years of age remained significant in the case of frontal vision limited to 120 degrees (F(1,53) = 5.22, p < 0.051, which constituted a very slight peripheral restriction. Moreover, the RLS was significant in 6-year-old children both with frontal vision limited to 60 degrees (t(31) = 4.64; p < 0.001) and with frontal vision limited to 120 degrees (t(31) = 2.04, p < 0.05). Either RLS,, or
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, , , , /, 345678
9
10
I, II
I+
AdUllS years
Fig. 3. Relative locomotor speed on narrow beam with frontal vision limited to 30, 60 and 120 degrees, calculated in comparison with the locomotor speed recorded with neutral spectacles (see the text), in the various age groups.
RLS120 no longer tended to increase with age from 8-9 years to adulthood. On the basis of these results, the strongest effects of PVR applied while walking as fast as possible on a narrow support were those observed in 6-year-old children. Discussion As already found to be the case in human adults (Assaiante et al. 1989) as well as in cats (Marchand and Amblard 1984, 1990; Marchand et al. 1990), the present study indicates that the locomotor speed
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is a good index to the difficulty of dynamic equilibrium in children. When the degree of locomotor equilibrium difficulty is increased by either narrowing the supporting surface or restricting the available visual information, the locomotor speed decreases. It is worth noting, however, that in human adults (Assaiante et al. 1989) as well as in cats (Marchand and Amblard 1990; Marchand et al. 1990) the locomotor speed can also reflect the difficulty of foot positioning while walking on an irregular terrain. Reducing the locomotor speed therefore appears to be the strategy generally used in response to any increase in the difficulty of a locomotor task, whether the difficulty involves dynamic equilibrium, foot positioning, visual restriction or fear of obstacles in darkness (Assaiante et al. 1989). Reducing the locomotor speed is certainly the easiest strategy to adopt in response to any locomotor difficulty, since 3-year-old children spontaneously use it when walking on the narrow beam for the first time. Walking on a narrow beam was in fact mastered by the children only after 3 years of age, that is to say about two years after the onset of unaided walking. At this stage, infants succeed in reducing the gap between their feet while walking (Bril and Breniere 1988; Breniere et al. 1989), thus reducing the supporting area, which shows that they have become able to master lateral equilibrium control while walking. In this experiment, we observed that the peripheral visual influence on locomotor equilibrium control did not vary monotonously as a function of age. Peripheral vision was found to play an important role in 3- to 6-year-old children, with a maximum influence at 6 years of age, whereas the use of these cues suddenly stopped in 7-year-old children, indicating a lack of interest for peripheral visual cues at this age. Their contribution again tended to increase from 8-9 years of age to adulthood. Our results confirm the effectiveness of the peripheral visual contribution to dynamic balance in adults (Assaiante et al. 19891, which is comparable to that observed in static balance (Amblard and Carblanc 1980; Paulus et al. 1984). The peripheral cues which intervene in balance control during locomotion, and which have already been assumed in adults to be dynamic visual cues (Assaiante et al. 19891, might be the same as those which putatively feed the rapid postural stabilization mechanism in man (Rezette and Amblard 1985; Amblard et al. 1985; Paulus et al. 1987). The optic flow induced by locomotion extends vertically as well as horizontally. Up to now, however, it has not been established whether
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the visual flow passing overhead and underhead of the observer is more or less useful for detecting and controlling egomotion than the flow passing on either side. Nevertheless, judging from our results, an intact peripheral flow along the frontal vertical does not suffice to compensate for the disruption induced by the various lateral peripheral barriers to the optical flow. We can hypothesize that a restriction of the optical flow including both the vertical and lateral periphery would have increased the difficulty of the locomotor task, if only because of the loss of sight of the supporting beam. As regards the effects of PVR on children, it would have been useful to know whether or not the size of the visual field changes with age. This question is still a matter of speculation, however (Whiteside 1976). Some authors have reported that no conspicuous variations in the visual field occur with age (Cohen and Haith 19771, while other authors have reported that a large increase in peripheral visual sensitivity occurs between the ages of 6 and 22 years (Lakowski and Aspinall 1969). Whiteside (1976), however, has suggested that the poor peripheral sensitivity in childhood described by the latter authors may have a conceptual or attentional rather than a perceptual basis. Moreover, it is also quite likely that this peripheral sensitivity may be fairly task-specific. Because of the discrepancies among studies on peripheral vision as a function of age, it is difficult to specify the contribution at various ages of peripheral vision to locomotor equilibrium control on the one hand, and the possible variations with age in the size of the visual field on the other hand. Moreover, the smallest PVR (120 degrees) impaired the relative speed in the 6-year-old children, but not in the 7-year-olds. This is unlikely to be attributable to some natural contraction of the visual field in the 7-year-old children in comparison with the 6-year-olds. Furthermore, we have noted a remarkable similarity between the effects of the severest (vision limited to 30 degrees) and the slightest (120 degrees) PVR as a function of age. This result suggests that the sudden lack of interest in peripheral visual cues in 7-year-old children is not limited to the extreme periphery of the visual field and therefore does not reflect any change in the size of the visual field. Moreover, all previous studies on visual perimeter have been based upon the conscious detection of visual stimuli, whereas the peripheral visual contribution to locomotor equilibrium control is presumably unconscious. We tend to agree with Stoffregen (personal
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communication, 1989) that it is not so much a question of age-related peripheral sensitivity, but rather one of how this sensitivity is used as a function of age and task. This point of view agrees very well with the early development of peripheral visual flow sensitivity demonstrated by Jouen and Lepecq in neonates (1989). Stoffregen (19851, however, adopting Gibson’s approach, has shown that postural stability is dependent on flow structure (radial or lamellar) rather than retinal projection as predicted classically by the peripheral dominance theory (Brandt et al. 1973). Lamellar flow presented to the centre of the retina therefore induced postural compensations, while radial flow to the periphery of the retina hardly did so at all. The present study was not designed to separate the effects of the flow structure from those pertaining to the source of retinal projection, but rather to restrict the lamellar flow naturally projected to the periphery of the retina during locomotion. The question therefore remains open, during some particular phases in the development of dynamic balance, as to whether peripheral dominance is restored or the effects of lamellar flow increase. It was observed in the present study that the sensitivity to peripheral optical flow in controlling locomotor equilibrium disappears transiently in 7-year-old children. The age of 6-7 years is therefore clearly a transition phase in the development of the peripheral visual control of locomotor equilibrium. This can be compared with other similar findings. At a more general level, it has already been reported that sensorimotor development is not linear in either childhood or babyhood (Hay 1987). Recent measurements of the neuromuscular response characteristics (Forssberg and Nashner 1982; Shumway-Cook and Woollacott 1985) have also shown that transition phases occur while children are refining their balance abilities. Shumway-Cook and Woollacott (1985) have reported that in 4- to 6-year-old children, the postural response organization deteriorates, and the response onset latencies become significantly more variable and longer than in 15 to 31-month-old infants, 7- to lo-year-old children or adults. On the other hand, Woollacott and colleagues (1987) have noted that 7-10year-old children, performing more stringent balance tasks no longer show adult-like automatic postural response characteristics. This result confirms that late improvements to visuo-postural and visuolocomotor skills occur during childhood. The question then arises as to how to interpret the dip in the
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contribution of peripheral vision to the maintenance of balance while walking on a beam at around 6-7 years. It seems unlikely in fact that this dip may have been simply due to sudden variations in the subjects’ sensory or motor abilities at the corresponding ages. On the one hand, we know that the sensory (proprioceptive, visual and vestibular) mechanisms involved in locomotor balance control have been quite mature for a long time at the age of 6-7 years. On the other hand, it has been reported that at this age the gait pattern, in terms of the EMG activity, no longer differs from that of adults (Berger 1986; B erger et al. 1988). The way in which the effects on peripheral visual cues on dynamic balance while walking vary with age during childhood does therefore seem to indicate that visuolocomotor control itself develops according to a non-monotonous pattern. There is an ongoing debate about the source of the perceptual information that controls and regulates balance. One view is that vision predominates over the other modalities when posture is perturbed in young children (Lee and Aronson 1974; Butterworth 1986). An alternative theory is that somatosensory, vestibular and visual control are all equally developed, but that when a yound child under 6 years of age is posturally disturbed he cannot produce an appropriate context-dependent weighting among the three modalities (Forssberg and Nashner 1982). According to Brandt et al. (19761, the irregular visual contribution to dynamic balance control abilities with age might reflect changes in some sequential, irregular and perhaps mutually interactive calibration between the visual and/or vestibular and proprioceptive loops which participate in the multisensory processes underlying locomotor balance control. This recalibration may take place for example at the age of 7, due to a sudden change in the centre of gravity arising from a growth spurt in the trunk which perturbs the optimal limb/trunk ratio required for walking to be stable (Sutherland et al. 1980). Woollacott (1988) has suggested rather that an apparent deterioration of the postural response characteristics may occur at a time when the child begins to integrate visual, vestibular and somatosensory inputs in balance control in order to adapt his or her postural responses to changing environmental conditions. We agree with this interpretation. We have reported elsewhere in fact that the beginning of effective use of the head stabilization in space strategy while walking on narrow supports occurred in 7-year-old children (Assaiante 1990). We sug-
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gested that from the age of 7-8 years onwards, an integrated signal specifying the head position relative to the supporting surface becomes progressively more available to the equilibrium control centers, thus allowing some freedom of the head with respect to the trunk. A similar hypothesis involving the availability of an integrated signal about the head position relative to the supporting surface was previously put forward in connection with standing adults (Lund and Broberg 1983). The apparent neglect of the peripheral visual cues in the locomotor control that we have described in the present experiment may correspond at 7 years of age to a re-weighting among the visual, vestibular and neck proprioception, which then become efficiently coordinated, resulting in an improved dynamic balance control. References Amblard, B. and A. Carblanc, 1980. Role of fovea1 and peripheral visual information in maintenance of postural equilibrium in man. Perception and Motor Skills 51, 903-912. Amblard, B., J. CrCmieux, A.R. Marchand and A. Carblanc, 1985. Lateral orientation and stabilization of human stance: Static versus dynamic visual cues. Experimental Brain Research 61, 21-37. Assaiante, C., 1990. Contrble visuel de l’equilibre locomoteur chez l’homme: Developpement et strategies sensori-matrices. Thesis, C.N.R.S., Universite Aix-Marseille II. Assaiante, C., B. Amblard and A. Carblanc, 1988. ‘Peripheral vision and dynamic equilibrium control in five to twelve year old children’. In: B. Amblard, A. Berthoz and F. Clarac (eds.), Posture and gait: Development, adaptation and modulation. Amsterdam: Elsevier. pp. 75-83. Assaiante, C. A.R. Marchand and B. Amblard, 1989. Discrete visual samples may control locomotor equilibrium and foot positioning in man. Journal of Motor Behavior 21, 72-91. Berger, W., 1986. ‘Development of gait in children’. In: W. Bles and Th. Brandt (eds.1, Disorders of posture and gait. Amsterdam: Elsevier. pp. 315-324. Berger, W., J. Quintern and V. Dietz, 1988. ‘Development of bilateral coordination of stance and gait in children’. In: B. Amblard, A. Berthoz and F. Clarac (eds.), Posture and gait: Development, adaptation and modulation. Amsterdam: Elsevier. pp. 67-74. Brandt, Th., J. Dichgans and E. Koenig, 1973. Differential effects of central versus peripheral vision on egocentric and exocentric motion perception. Experimental Brain Research 16, 476-491. Brandt, T., D. Wenzel and J. Dichgans, 1976. Die Entwicklung der visuellen Stabilisation des aufrechten Standes beim Kind: Ein Reifezeichen in der Kinderneurologie. Archiv fiir Psychiatric und Nervenkrankheiten 223, 1-13. Breniere, Y., B. Bril and R. Fontaine, 1989. Analysis of the transition from upright stance to steady-state locomotion in children with under 200 days of autonomous walking. Journal of Motor Behavior 21, 20-37. Bril, B. and Y. Brenibre, 1988. ‘Do temporal invariances exist as early as the first six months of independent walking?’ In: B. Amblard, A. Berthoz, F. Clarac (eds.1, Posture and gait: Development, adaptation and modulation. Amsterdam: Elsevier. pp. 23-31. Butterworth, G., 1986. In: M. Wade and H. Whiting (eds.1, Motor development in children: Aspects of coordination and control. Dordrecht: Martinus Nijhoff.
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balance
Butterworth, G. and L. Hicks, 1977. Visual proprioception and postural stability in infancy. A developmental study. Perception 6, 255-262. Cohen, K.M. and M.M.J. Haith, 1977. Peripheral vision: The effects of developmental, perceptual, and cognitive factors. Experimental Child Psychology 24. 373-394. Forssberg, H. and L.M. Nashner, 1982. Ontogenic development of postural control in man: Adaptation to altered support and visual conditions during stance. The Journal of Neuroscience 2, 545-552. Hay. I., 1987. Etude ontogenetique du controle d’un mouvement: L’approche manuelle. Thesis, Centre de Documentation CNRS-GLM, Aix-Marseille II. Jouen, F., 1986. La contribution des recepteurs visuels et labyrinthiques a la detection des d&placements du corps propre chez le nom&on. L’annee psychologique 86, 169-182. Jouen, F. and J.C. Lepecq, 1989. La sensibilite au flux optique chez le nouveau-m? Psychologie Frangaise. Le contrc”lle visuel des d&placements 34, 13-18. Lakowski, R. and P. Aspinall, 1969. Static perimetry in young children. Vision Research 9, 305-312. Lee, D. and E. Aronson. 1974. Visual proprioceptive control of standing in human infants, Perception and Psychophysics 15, 529-532. Lund, S. and C. Broberg. 1983. Effects of different head positions on postural sway in man induced by a reproducible vestibular error signal. Acta Physiol. Stand. 117, 307-309. Marchand. A.R. and B. Amblard, 1984. Locomotion in adult cats with early vestibular deprivation: Visual cue substitution. Experimental Brain Research 54, 395-405. Marchand. A.R. and B. Amblard, 1990. Early sensory determinants of locomotor speed in adult cats: 1. Visual compensation after bilabyrinthectomy in cats and kittens. Behavioral Brain Research 37, 215-225. Marchand, A.R., J. Cremieux and B. Amblard, 1990. Early sensory determinants of locomotor speed in adult cats: II. Effects of strobe rearing on vestibular functions. Behavioral Brain Research 37, 227-235. Owen. B.M. and D.N. Lee, 1986. ‘Establishing a frame of reference for action’. In: M. Wade and H. Whiting teds.), Motor development in children: Aspects of coordination and control. Dordrecht: Martinus Nijhoff. pp. 2X7-308 Paulus. W.M., A. Straube and T. Brandt. 1984. Visual stabilization of posture. Physiological stimulus characteristics and clinical aspects. Brain 107, 1143-l 163. Paulus, W.M., A. Straube and T. Brand& 1987. Visual postural performance after loss of somatosensory and vestibular function. Journal of Neurology, Neurosurgery, and Psychiatry. SO, 1542-1545. RCzette, D. and B. Amblard, 1985. Orientation versus motion visual cues to control sensorimotor skills in some acrobatic leaps. Human Movement Science 4, 2977306. Shumway-Cook, A. and M. Woollacott, 1985. The growth of stability: Postural control from a developmental perspective. Journal of Motor Behavior 17, 131-147. Stoffregen, T.A., 1985. Flow structure versus retinal location in the optical control of stance. J. Exp. Psychol.: Human Perception and Performance 11, 554-566. Stoffregen. T.A., M.A. Schmuckler and E.J. Gibson, 1987. Use of central and peripheral optical flow in stance and locomotion in young walkers. Perception 16, 113-l 19. Sutherland, D.H.. R. Olshen, L. Cooper and S.L. Woo, 1980. The development of mature gait. Journal of Bone and Joint Surgery 62, 3366353. Whiteside, J.A., 1976. Peripheral vision in children and adults. Child Development 47, 290-293. Woollacott, M.H., 1988. ‘Posture and gait from newborn to elderly’. In: B. Amblard, A. Berthoz and F. Clarac teds.). Posture and gait: Development, adaptation and modulation. Amsterdam: Elsevier. pp. 3-12. Woollacott, M.H.. B. Debu and M. Mowatt, 1987. Neuromuscular control of posture in the infant and child: Is vision dominant‘? Journal of Motor Behavior 19, 167-186.
Science
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11 (1992) 533-548
Peripheral vision and age-related differences in dynamic balance C. Assaiante Laboratoire
and B. Amblard
de Neurosciences
*
Fonctionnelles,
CNRS, Marseille, France
Abstract
Assaiante, C. and B. Amblard, 1992. Peripheral balance. Human Movement Science 11, 533-548.
vision and age-related
differences
in dynamic
The purpose of this study was to investigate the role of peripheral visual cues in locomotor equilibrium as a function of age in 3- to 12.year-old children and adults. Peripheral visual restrictions (PVR), limiting frontal vision to either 30, 60 or 120 degrees, were applied to subjects walking on a narrow beam. The subjects’ locomotor equilibrium performances were evaluated in terms of the locomotor speed, which constitutes a good index to the difficulty of locomotor balancing. The results showed that the influence of peripheral visual cues on locomotor equilibrium control did not vary monotonously with age. The peripheral visual contribution to dynamic balance control increased from 3 to 6 years of age, with a maximum in h-year-old children. The peripheral visual influence on locomotor equilibrium control then disappeared suddenly in the 7-year-old children. It tended to increase again from 8-9 years of age to adulthood. In adults, the peripheral visual contribution to locomotor equilibrium that we have described previously was confirmed and compared to that involved in postural control. It is concluded from these results that late improvements occur in locomotor balance control during childhood.
Introduction Peripheral visual cues as well as motion visual cues have been reported to play a particularly important role in the control of postural (Amblard and Carblanc 1980; Paulus et al. 1984; Amblard et * We are grateful to Bernard Assaiante revising the English. Correspondence to: C. Assaiante, UPR 13402 Marseille-Ctdex 9, France.
0167-9457/92/$05.00
0 1992 - Elsevier
for iconographic
assistance
de Neurobiologie
Science
Publishers
and to Dr. Jessica
et Mouvements
B.V. All rights
du CNRS,
reserved
Blanc for B.P. 71,
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al. 1985; Stoffregen 1985) as well as locomotor equilibrium in adults (Assaiante et al. 1989; Assaiante 1990). Some studies on babies (Jouen 1986) and young children (Lee and Aronson 1974; Brandt et al. 1976; Butter-worth and Hicks 1977; Stoffregen et al. 1987) have also indicated that visual, particularly peripheral cues, play a prominent role in the elaboration and control of static postural equilibrium. It has been reported moreover that vision predominates in infants during transitional periods in which they attempt to master new postural challenges (Butterworth 1986). It has been observed that the sensitivity to visual flow increases as the infants learn to sit without support (Butterworth and Hicks 1977). This sensitivity increases again with the onset of upright stance (Lee and Aronson 1974) and with the onset of unaided walking (Stoffregen et al. 1987). These transition phases are not restricted to babyhood, however. Recent studies (Shumway-Cook and Woollacott 1985) have shown that a transition phase in postural development occurs in 4- to 6-year-old children, which suggests that postural control improvements continue to take place during childhood and that some changes with age in the use of visual cues can probably be observed. Up to now, developmental studies have focused particularly on the visual contribution to static postural equilibrium, but very little attention has been paid to the changes in the use of visual cues in locomotor equilibrium control as a function of age. Owen and Lee (1986) have reported that 3- to 5-year-old walkers showed body oscillations in response to an optical flow, artificially induced with a moving room. Stoffregen et al. (1987) also reported that in young walkers (up to 5 years of age) an optical flow, artificially induced with a moving room and presented only to the periphery of the visual field, resulted in a higher level of compensatory postural responses than when centrally presented. According to these authors, this difference resulted from the dynamic geometrical structure of the optical flow normally associated with locomotion. This structure is radial in the center of the optical flow and lamellar in its periphery. Stoffregen et al. concluded that children in the age range 2-5 years show the same relative sensitivity as adults to the dynamic structure of the peripheral optic array in controlling posture. The main purpose of the present study was to examine the developmental changes in the use made of peripheral visual cues from the natural optical flow associated with locomotion in controlling balance
C. Assaiante, B. Amblard / Peripheral L,isionand dynamic balance
535
during walking, in 3- to 12-year-old children. In order to specifically test the lateral equilibrium component of locomotion, we asked our young subjects to walk on a narrow beam. We have previously reported that this locomotor task actually produced an enhancement of the body sway in the frontal plane, attesting to an increase in the level of lateral equilibrium difficulty (Assaiante 1990). In order to evaluate the contribution of visual factors to balance control while walking on a narrow beam, we subjected the subjects to peripheral visual cue restrictions. The peripheral visual field was variably restricted by means of appropriate spectables limiting vision to the frontal field (Assaiante et al. 19881. The subjects’ performances were evaluated by simply measuring the locomotor speed on narrow supports, which has been previously shown to be highly sensitive to the supplementary difficulty of maintaining dynamic lateral equilibrium encountered under restricted visual conditions, in both animals (Marchand and Amblard 1984, 1990) and humans (Assaiante et al. 1989).
Methods Subjects Two hundred and fifteen normal healthy children from 3 to 12 years of age participated in this experiment. The youngest were recruited from a nursery school and the others from a primary school. Ten groups of subjects were formed on the basis of their age (for example, ‘age 3’ contained 2.5 to 3.5year-old children). From youngest to oldest, these ten age groups consisted of twenty-four, twenty-nine, twenty-four, thirty-two, twenty-three, twenty-three, twenty-five, twenty-two, eight and five children, respectively. The same groups included fifteen, nineteen, nine, fifteen, twelve, fifteen, thirteen, twelve, three and four males, respectively. A control group consisting of twelve healthy adults, five women and seven men aged from 20 to 45 years underwent the same experiment. Tasks and surroundings The experiment was performed in a primary school gymnasium (30 m wide, 45 m in length) providing the children with a familiar
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C. Assaiante, B. Amblard / Peripheral Ii.kn and dynamic baiunce
environment. Locomotor equilibrium was studied on a narrow support (wooden beam, 10 cm wide, 20 cm high, 6 m long). The locomotor speed was measured by means of an infrared optical device and an electronic timer, over a distance of 5 m excluding the first 50 and the last 50 cm of the total beam length to eliminate the initial acceleration and final deceleration. The infrared optical device did not involve any cable being attached to the subjects, who were totally free to walk on the beam. The subjects had to walk as fast as possible on the beam. When the subjects lost balance during a trial, they were requested to perform another trial until they succeeded under the same experimental conditions. These falls were independent of the visual conditions and almost were no longer observed from 4-5 years of age onwards.
Visual conditions Peripheral visual restrictions (PVR) were applied by means of appropriate spectacles. The neutral glasses of these spectacles were partly covered with black adhesive tape, in such a way that vision was possible only through a central vertical slit in front of each eye. The widths of these slits were chosen so as to obtain binocular central visual fields of either 30, 60, or 120 degrees. Complementary black protective devices were used around the frames of the spectacles to avoid undesirable lateral vision. Whatever the PVR, the locomotor support always remained visible in front of the subject. Moreover, two control situations were included: normal vision (NV) (without spectacles) and vision through neutral spectacles (NS) without any other visual limitations.
Experimental session Either four to six children or two adults were tested at each session. Under a given visual condition, they performed the task in turn so that each was able to rest between his own successive trials. With each visual condition, the locomotor task was run twice according to a pseudo-random plan, and the results of the two trials performed by each subject were averaged.
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537
Analysis The speed values were converted into logarithms and the results obtained with all the subjects in each age group were pooled for the graphs. A log scale was preferred to a linear scale in the figures because it shows up the relative rather than the absolute changes in speed depending on the visual conditions, and therefore yields comparable dispersions over a wide range of absolute speeds (Marchand and Amblard 1984, 1990; Assaiante et al. 1989). The log transform of speed was also used for the statistics because the comparisons involved a wide range of absolute speeds, with some of the values approaching the lower limit (zero speed). In view of the variations in the number of subjects from one group to another, an appropriate ANOVA program VAR3 ’ was used to test the degree of significance of the comparisons made between experimental situations. A regression analysis was also carried out to test the changes with age in the locomotor speed under normal vision. Lastly, with each age group and visual condition, the relative loss of speed (see below) was used in a one-sample analysis (t-statistic) against the null hypothesis (STATGRAPHICS program).
Results The individual locomotor speeds while walking on a narrow beam under normal vision (fig. l), in 3- to 12-year-old children and in adults, were subjected to a regression analysis. It can be seen from this figure that the mean speed increased quite regularly with age in the 3- to 9-year-old children with a fairly sharp slope (0.285 + 0.010, with t = 26.11); whereas it almost reached a plateau from the age of 9 up to adulthood, as attested by the very gentle slope (0.012 f 0.008, with t = 1.45). Moreover, the individual variations in locomotor speed under normal vision did not show any clearly detectable changes with age, as attested in fig. 1 by the roughly constant dispersion. The average locomotor speed while walking on a narrow beam under various visual conditions is shown in log scale in fig. 2, in 3- to ’ Rouanet, report.
P., M.O.
Lebeaux
and
D. Ltpine,
Programme
VAR3,
Univ.
of Paris
6, Internal
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C. Assaiante, B. Amblard / Peripheral vision and dynamic balance /
I
I
I
I
J
I
I
I
I
e
5
10
15
20
1 a5
AGE(years) Fig. 1. Individual locomotor speed while walking on a narrow beam under normal vision as a function of age. The two straight lines result from linear regression analyses of speed versus age in the 3- to 9-year-old (left side) and Y-year-old to adult age groups (right side).
12-year-old children and in adults. The mean locomotor speed was highly dependent upon the subjects’ age (F(8, 16.5) = 38.9, p < 0.001) under all the visual conditions. Within a given age group, the effects of the visual factor (5 visual conditions) were significant in all the age groups, except in the 12-year-old children (see details in table 1). These results confirmed that peripheral vision is used to control lateral dynamic equilibrium in childhood, at least while walking on a narrow support. The curves in fig. 2, which are roughly parallel, suggest that peripheral visual restrictions induced relative rather than absolute changes in the locomotor speed. It can be seen moreover from fig. 2 that these relative changes in speed depending on the visual conditions differed among the
C. Assaiante, B. Amblard / Peripheral uision and dynamic balance
1 30
I
I
1
4
60
vm
ws
NV
Fig. 2. Mean locomotor speed on narrow beam as function of age (in years; ad: adults) conditions: frontal vision limited to 30, 60 or 120 degrees; neutral spectacles without field limitation (NS); normal vision without spectacles (NV).
539
and visual any visual
various age groups studied, which indicates that the way in which PVR influenced the locomotor speed depended upon the subjects’ age. In order to specify this effect, we have calculated the ‘relative speed’ RS, obtained under each PVRi condition (i = 30, 60 or 120) by comparing the absolute speed (Si> (but not its log transform) obtained under PVRi with the speed (S,,) obtained with neutral spectacles: RS, = 100 - (S,,
- S,)/S,,
= 100 - RLS,,
where RLSi was the ‘relative loss of speed’ due to PVR,. The latter visual condition S,, was chosen as a control situation in order to
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B. Amblard
/ Peripherul lision and dynamic balance
Table 1 Significance levels determined by applying ANOVA to the visual effects on the locomotor speed (second column) and by performing one-sample analysis (t-statistic) to the relative loss of speed in the case of frontal vision limited to 30 degrees (third column). Age group 3 years 4 years 5 years 6 years 7 years 8 years 9 years 10 years 11 years 12 years Adults
Visual effects
RLS,n
F(4,92) = 8.98 p < 0.001 F(4.112) = 6.39 p < 0.001 F(4.92) = 7.30 p < 0.001 F(4,124)= 15.42 p < 0.001 F(4,88) = 4.96 p < 0.01 F(4.88) = 3.14 p < 0.05 F(4.96) = 16.03 p < 0.001 F(4,84) = 5.91 p < 0.001 F(4,28) = 8.76 p < 0.001
t(23) = 2.63 p < 0.05 t(28) = 2.21 p < 0.05
tl.S.
F(4,44) = 4.97 p < 0.01
“.S.
t(31) = 6.96 p < 0.001 n.s. “.S.
t(24) = 2.96 p < 0.01 “.S. t(7) = 2.98 p < 0.05 n.s. t(11)= 3.83 p < 0.01
avoid the artefacts induced by spectable wearing in children who are not accustomed to wearing spectacles. We often observed significant differences in mean locomotor speed between normal vision (NV) and neutral spectacle (NS) conditions, as can be seen from table 2. There seems to be no obvious explanation for this phenomenon. The relative speed corresponding to each of the three PVR conditions is presented in fig. 3 as a function of the subjects’ age. The severest visual restriction naturally induced the greatest loss of speed in comparison with the normal spectacle-wearing conditions. The relative loss of speed due to frontal vision being limited to 30 degrees was significant in most of the age groups (see details in table 1). RLS,, was maximum in 6-year-old children: the relative speed RS,, was in fact lower in the 6-year-olds than in the 5-year-olds (F(1.54) = 4.4, p < 0.05), and was also lower in the 6-year-olds than in the 7-year-olds (F(1,53) = 10.9, p < 0.01). Moreover, little difference in speed was
C. Assaiante. B. Amblard / Peripheral rision and dynamic balance Table
541
2
Significance levels determined by applying between neutral spectacles (NS) and normal Age group
3 years 4 years 5 years 6 years 7 years 8 years 9 years 10 years 11 years 12 years Adults
ANOVA to the differences visual (NV) conditions.
in locomotor
speed
Difference between NS and NV conditions F(1,23) = 7.07 p < 0.05 F(1,28) = 4.49 p < 0.05 F(1,23) = 7.88 p < 0.01 n.s. F(1,22) = 4.30 p < 0.05 F(1,22) = 7.94 p < 0.01 F(1,24) = 14.03 p < 0.001 F(1,21) = 4.32 p < 0.05 F&7) = 12.25 p < 0.01 n.s. n.s.
observed between the 30 degrees and neutral spectacles conditions in the 7-year-old subjects, but thereafter this difference tended to increase with age (p < 0.07) up to adulthood, when this difference becomes very significant (see details in table 1). The latter result confirmed the importance of peripheral vision in controlling locomotor equilibrium in adults (Assaiante et al. 1989). Considerable similarity exists between the three curves in fig, 3 from 4 years of age to adulthood. Indeed, in the case of frontal vision limited to 60 degrees, significant differences in RS,, were again observed both between 5 and 6 years of age (F(1,54) = 4.95, p < 0.05) and between 6 and 7 years of age (F(1,53) = 12.20, p < 0.001). The RS difference between 6 and 7 years of age remained significant in the case of frontal vision limited to 120 degrees (F(1,53) = 5.22, p < 0.051, which constituted a very slight peripheral restriction. Moreover, the RLS was significant in 6-year-old children both with frontal vision limited to 60 degrees (t(31) = 4.64; p < 0.001) and with frontal vision limited to 120 degrees (t(31) = 2.04, p < 0.05). Either RLS,, or
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C. Assaiante, B. Amblard / Peripheral rision and dynamic balance
, , , , /, 345678
9
10
I, II
I+
AdUllS years
Fig. 3. Relative locomotor speed on narrow beam with frontal vision limited to 30, 60 and 120 degrees, calculated in comparison with the locomotor speed recorded with neutral spectacles (see the text), in the various age groups.
RLS120 no longer tended to increase with age from 8-9 years to adulthood. On the basis of these results, the strongest effects of PVR applied while walking as fast as possible on a narrow support were those observed in 6-year-old children. Discussion As already found to be the case in human adults (Assaiante et al. 1989) as well as in cats (Marchand and Amblard 1984, 1990; Marchand et al. 1990), the present study indicates that the locomotor speed
C. Assaiante, B. Amblard / Peripheral vision and dynamic balance
543
is a good index to the difficulty of dynamic equilibrium in children. When the degree of locomotor equilibrium difficulty is increased by either narrowing the supporting surface or restricting the available visual information, the locomotor speed decreases. It is worth noting, however, that in human adults (Assaiante et al. 1989) as well as in cats (Marchand and Amblard 1990; Marchand et al. 1990) the locomotor speed can also reflect the difficulty of foot positioning while walking on an irregular terrain. Reducing the locomotor speed therefore appears to be the strategy generally used in response to any increase in the difficulty of a locomotor task, whether the difficulty involves dynamic equilibrium, foot positioning, visual restriction or fear of obstacles in darkness (Assaiante et al. 1989). Reducing the locomotor speed is certainly the easiest strategy to adopt in response to any locomotor difficulty, since 3-year-old children spontaneously use it when walking on the narrow beam for the first time. Walking on a narrow beam was in fact mastered by the children only after 3 years of age, that is to say about two years after the onset of unaided walking. At this stage, infants succeed in reducing the gap between their feet while walking (Bril and Breniere 1988; Breniere et al. 1989), thus reducing the supporting area, which shows that they have become able to master lateral equilibrium control while walking. In this experiment, we observed that the peripheral visual influence on locomotor equilibrium control did not vary monotonously as a function of age. Peripheral vision was found to play an important role in 3- to 6-year-old children, with a maximum influence at 6 years of age, whereas the use of these cues suddenly stopped in 7-year-old children, indicating a lack of interest for peripheral visual cues at this age. Their contribution again tended to increase from 8-9 years of age to adulthood. Our results confirm the effectiveness of the peripheral visual contribution to dynamic balance in adults (Assaiante et al. 19891, which is comparable to that observed in static balance (Amblard and Carblanc 1980; Paulus et al. 1984). The peripheral cues which intervene in balance control during locomotion, and which have already been assumed in adults to be dynamic visual cues (Assaiante et al. 19891, might be the same as those which putatively feed the rapid postural stabilization mechanism in man (Rezette and Amblard 1985; Amblard et al. 1985; Paulus et al. 1987). The optic flow induced by locomotion extends vertically as well as horizontally. Up to now, however, it has not been established whether
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the visual flow passing overhead and underhead of the observer is more or less useful for detecting and controlling egomotion than the flow passing on either side. Nevertheless, judging from our results, an intact peripheral flow along the frontal vertical does not suffice to compensate for the disruption induced by the various lateral peripheral barriers to the optical flow. We can hypothesize that a restriction of the optical flow including both the vertical and lateral periphery would have increased the difficulty of the locomotor task, if only because of the loss of sight of the supporting beam. As regards the effects of PVR on children, it would have been useful to know whether or not the size of the visual field changes with age. This question is still a matter of speculation, however (Whiteside 1976). Some authors have reported that no conspicuous variations in the visual field occur with age (Cohen and Haith 19771, while other authors have reported that a large increase in peripheral visual sensitivity occurs between the ages of 6 and 22 years (Lakowski and Aspinall 1969). Whiteside (1976), however, has suggested that the poor peripheral sensitivity in childhood described by the latter authors may have a conceptual or attentional rather than a perceptual basis. Moreover, it is also quite likely that this peripheral sensitivity may be fairly task-specific. Because of the discrepancies among studies on peripheral vision as a function of age, it is difficult to specify the contribution at various ages of peripheral vision to locomotor equilibrium control on the one hand, and the possible variations with age in the size of the visual field on the other hand. Moreover, the smallest PVR (120 degrees) impaired the relative speed in the 6-year-old children, but not in the 7-year-olds. This is unlikely to be attributable to some natural contraction of the visual field in the 7-year-old children in comparison with the 6-year-olds. Furthermore, we have noted a remarkable similarity between the effects of the severest (vision limited to 30 degrees) and the slightest (120 degrees) PVR as a function of age. This result suggests that the sudden lack of interest in peripheral visual cues in 7-year-old children is not limited to the extreme periphery of the visual field and therefore does not reflect any change in the size of the visual field. Moreover, all previous studies on visual perimeter have been based upon the conscious detection of visual stimuli, whereas the peripheral visual contribution to locomotor equilibrium control is presumably unconscious. We tend to agree with Stoffregen (personal
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communication, 1989) that it is not so much a question of age-related peripheral sensitivity, but rather one of how this sensitivity is used as a function of age and task. This point of view agrees very well with the early development of peripheral visual flow sensitivity demonstrated by Jouen and Lepecq in neonates (1989). Stoffregen (19851, however, adopting Gibson’s approach, has shown that postural stability is dependent on flow structure (radial or lamellar) rather than retinal projection as predicted classically by the peripheral dominance theory (Brandt et al. 1973). Lamellar flow presented to the centre of the retina therefore induced postural compensations, while radial flow to the periphery of the retina hardly did so at all. The present study was not designed to separate the effects of the flow structure from those pertaining to the source of retinal projection, but rather to restrict the lamellar flow naturally projected to the periphery of the retina during locomotion. The question therefore remains open, during some particular phases in the development of dynamic balance, as to whether peripheral dominance is restored or the effects of lamellar flow increase. It was observed in the present study that the sensitivity to peripheral optical flow in controlling locomotor equilibrium disappears transiently in 7-year-old children. The age of 6-7 years is therefore clearly a transition phase in the development of the peripheral visual control of locomotor equilibrium. This can be compared with other similar findings. At a more general level, it has already been reported that sensorimotor development is not linear in either childhood or babyhood (Hay 1987). Recent measurements of the neuromuscular response characteristics (Forssberg and Nashner 1982; Shumway-Cook and Woollacott 1985) have also shown that transition phases occur while children are refining their balance abilities. Shumway-Cook and Woollacott (1985) have reported that in 4- to 6-year-old children, the postural response organization deteriorates, and the response onset latencies become significantly more variable and longer than in 15 to 31-month-old infants, 7- to lo-year-old children or adults. On the other hand, Woollacott and colleagues (1987) have noted that 7-10year-old children, performing more stringent balance tasks no longer show adult-like automatic postural response characteristics. This result confirms that late improvements to visuo-postural and visuolocomotor skills occur during childhood. The question then arises as to how to interpret the dip in the
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contribution of peripheral vision to the maintenance of balance while walking on a beam at around 6-7 years. It seems unlikely in fact that this dip may have been simply due to sudden variations in the subjects’ sensory or motor abilities at the corresponding ages. On the one hand, we know that the sensory (proprioceptive, visual and vestibular) mechanisms involved in locomotor balance control have been quite mature for a long time at the age of 6-7 years. On the other hand, it has been reported that at this age the gait pattern, in terms of the EMG activity, no longer differs from that of adults (Berger 1986; B erger et al. 1988). The way in which the effects on peripheral visual cues on dynamic balance while walking vary with age during childhood does therefore seem to indicate that visuolocomotor control itself develops according to a non-monotonous pattern. There is an ongoing debate about the source of the perceptual information that controls and regulates balance. One view is that vision predominates over the other modalities when posture is perturbed in young children (Lee and Aronson 1974; Butterworth 1986). An alternative theory is that somatosensory, vestibular and visual control are all equally developed, but that when a yound child under 6 years of age is posturally disturbed he cannot produce an appropriate context-dependent weighting among the three modalities (Forssberg and Nashner 1982). According to Brandt et al. (19761, the irregular visual contribution to dynamic balance control abilities with age might reflect changes in some sequential, irregular and perhaps mutually interactive calibration between the visual and/or vestibular and proprioceptive loops which participate in the multisensory processes underlying locomotor balance control. This recalibration may take place for example at the age of 7, due to a sudden change in the centre of gravity arising from a growth spurt in the trunk which perturbs the optimal limb/trunk ratio required for walking to be stable (Sutherland et al. 1980). Woollacott (1988) has suggested rather that an apparent deterioration of the postural response characteristics may occur at a time when the child begins to integrate visual, vestibular and somatosensory inputs in balance control in order to adapt his or her postural responses to changing environmental conditions. We agree with this interpretation. We have reported elsewhere in fact that the beginning of effective use of the head stabilization in space strategy while walking on narrow supports occurred in 7-year-old children (Assaiante 1990). We sug-
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