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Postural control in children with strabismus: Effect of eye surgery
Neuroscience Letters 501 (2011) 96–101
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Postural control in children with strabismus: Effect of eye surgery Agathe Legrand a,∗ , Emmanuel Bui Quoc b,c , Sylvette Wiener Vacher d , Jérôme Ribot c , Nicolas Lebas c , Chantal Milleret c , Maria Pia Bucci a a
Laboratoire de Psychologie et Neuropsychologie Cognitives, FRE 3292 CNRS IUPDP Université Paris Descartes, 71 Avenue Edouard Vaillant, 92774 Boulogne Billancourt Cedex, France Ophthalmology Department, Hôpital Robert Debré, 48 Boulevard Sérurier, 75019 Paris, France Laboratoire de Physiologie de la Perception et de l’Action, Collège de France, CNRS UMR 7152, 11 place Marcelin Berthelot, 75005 Paris, France d Ear Nose Throat and Cervico Facial Surgery Department, Hôpital Robert Debré, 48 Boulevard Sérurier, 75019 Paris, France b c
a r t i c l e
i n f o
Article history: Received 22 April 2011 Received in revised form 8 June 2011 Accepted 30 June 2011 Keywords: Children Strabismus Eye surgery Postural stability
a b s t r a c t The purpose of this study was to examine the postural control in children with strabismus before and after eye surgery. Control of posture is a complex multi-sensorial process relying on visual, vestibular and proprioceptive systems. Reduced influence of one of such systems leads to postural adaptation due to a compensation of one of the other systems [3]. Nine children with strabismus (4–8 years old) participated in the study. Ophthalmologic, orthoptic, vestibular and postural tests were done before and twice (2 and 8 weeks) after eye surgery. Postural stability was measured by a platform (TechnoConcept): two components of the optic flux were used for stimulation (contraction and expansion) and two conditions were tested eyes open and eyes closed. The surface area of the center of pressure (CoP), the variance of speed of the CoP and the frequency spectrum of the platform oscillations by fast Fourier transformation were analysed. Before surgery, similar to typically developing children, postural stability was better in the eyes open condition. The frequency analysis revealed that for the low frequency band more energy was spent in the antero-posterior direction compared to the medio-lateral one while the opposite occurred for the middle and the high frequency bands. After surgery, the eye deviation was reduced in all children and their postural stability also improved. However, the energy of the high frequency band in the mediolateral direction increased significantly. These findings suggest that eye surgery influences somatosensory properties of extra-ocular muscles leading to improvement of postural control and that binocular visual perception could influence the whole body. © 2011 Elsevier Ireland Ltd. All rights reserved.
Posture involves a coordinated relationship of the different segments of the body. It promotes balance, which is the ability to maintain a stable condition at any time. Control of posture is a complex process based on multiple interactions among visual, vestibular and proprioceptive sensory systems. Reducing the influence of one system leads to postural adaptation due to a compensation by one of the other systems [3]. As described by Assaiante et al. [1], the development of postural control takes place during the growth of the child. The child builds a repertoire of postural strategies. Subsequently, he must learn to choose the best strategy in a situation of imbalance. By examining postural stability in 140 children aged 3–16 years, Steindl et al. [25] suggested that a child only reaches postural maturation at about 10 years of age. There is therefore a strong interaction between postural control and age (but no gender difference). Postural control has long been regarded as an automatic response. But recent studies have shown the existence of a pos-
∗ Corresponding author. E-mail address: [email protected] (A. Legrand). 0304-3940/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2011.06.056
ture regulation process, both in case of a simple task or a more complicated one, involving several attention processes [2]. The mobilization of such attentional sources is dependent on many factors such as the age, availability of sensory information, the complexity of the task and postural skills. In this regard, Olivier et al. [18,19] showed an effect of attention on body sway depending on age. From their data, they suggested that the mature level of attention was not reached before 11 years old. Furthermore, it appeared that both children and adults had to concentrate their attention and to spend energy to reach good postural stability. Quantifications of postural stability on a fixed or a movable surface in 7–12 year old children revealed an increase of body sway in case of a moving surface [23]. Similarly, in a dynamically moving scene, for example, after presentation of a stimulus reproducing optical flow (by alternating concentric circles of black and white or black and white squares), the maintenance of standing in children was shown to be more difficult than in the adult. This was due to the involvement of two conflicting sensory inputs: some visual and some vestibular. They emphasized that the conflict of sensory inputs is difficult to manage for the young child. This is strengthened by the fact that children are particularly visually dependent
A. Legrand et al. / Neuroscience Letters 501 (2011) 96–101
(more than the adults are). Indeed, it is well known that vision plays a major role in postural control in children: to closure their eyes greatly impairs balance. This indicates that visual information is one of the most important sources for postural stabilization [22]. As a consequence, a dysfunction of visual input in children might induce difficulties in maintaining proper postural balance. But surprisingly this has been as yet only poorly investigated. In about 4% of young population sensory and/or motor pathways are not correctly developed leading to a misalignment of the visual axis and strabismus. Strabismus eye surgery is one of the methods used for treatment [26]. Studies examining the relationship between strabismus and posture are very scarce. From our knowledge at least, there are only two. First, more than twenty years ago, a Swedish study reported that the presence of exotropia was accompanied by greater body sways [17]. Second, more recently, a study was conducted in Japan [14] on postural balance in strabismic children from 3 to 12 years before and after surgery. These authors reported greater postural instability after strabismus surgery than before, whether the eyes were kept open or closed. Importantly, children with binocular capabilities were more stable after surgery than children having no stereopsis. Unfortunately, data obtained before surgery in the conditions eyes open and eyes closed were not compared each other. Another important point may be critical. Posture was recorded 3 days after surgery while anesthetic may still have some effects on the body, and therefore on the proprioception of extraocular muscles [28]. In the present study, we examined the quality of postural control before and after strabismus surgery. After surgery, performances were compared after two different postsurgery delays: 2 weeks and 2 months. Posture was quantified while children were looking at some components of the optic flow (contraction vs. expansion). Our choice was guided by the fact that perception of movement is known to be impaired in strabismic amblyopic subjects only [11,12]. In accordance with Matsuo et al. [14], we expected to find poor postural control, at least in the post 1 surgery condition, because of the proprioceptive changes in the extra-ocular muscles [6]. In the post 2 surgery condition, stability of children could be improved via adaptive mechanisms. Nine strabismic children between 4 and 8 years old participated in the study. The investigation adhered to the principles of the Declaration of Helsinki and was approved by our institutional Human Experimentation Committee. Informed parental consent was obtained for each subject after the nature of the procedure had been explained. Prior to surgey all children underwent a complete ophthalmological, orthoptic and vestibular examination. Global vestibular and proprioception evaluation was done using two clinical tests: the Romberg eye open and closed and the Halmagyi tests or head thrust test. The Romberg test is performed by asking the child to stand, feet close to each other and arms along the trunk with eyes open and eyes closed, on a hard surface and a soft surface (mattress). The child was asked to stand quietly in this position for 20 s with a minimal sway. The Head thrust test [9] evaluates the function of the semicircular canals of the vestibular receptors. The head is rotated passively and briefly on the planes of a semicircular canals while the child is asked to fixate a target placed at 60 cm from him. A right horizontal head rotation evaluates the function of the right semicircular canal, to the left for the left horizontal canal. The eyes can stay on the target in such a rapid head movement only if the canal tested is functional. If the canal is not functional the eyes are first moving with the head during the head rotation and then making a rapid saccade to bring back the gaze on the target: this catch up saccade indicates a deficit of the corresponding canal. A normal clinical Halmagyi test without catch up saccade indicates a normal vestibular canal func-
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tion. In our study all children had a normal Romberg and Halmagyi test. Clinical data of each child are shown in Table 1. Seven children (C1, C3, C5, C6, C7, C8 and C9) had convergent strabismus (esotropia): more precisely, four of them (C3, C5, C6 and C8) had infantile esotropia, two children (C1 and C7) had partially accommodative esotropia and one child only (C9) had secondary esotropia. The other two children (C2 and C4) had divergent strabismus (exotropia). Binocular visual capability was assessed with the TNO test and no child showed stereopsis. All children underwent strabismus surgery. Two children (C1 and C7) underwent bilateral medial rectus recession (3–4 mm) combined with the Cüppers technique; one child (C9) underwent bilateral medial rectus recession (8 mm); four children (C3, C5, C6 and C8) underwent medial rectus recession (4–7 mm) combined with lateral rectus resection (4–7 mm) and two children (C2 and C4) underwent lateral rectus recession (6 mm) combined with medial rectus resection (7 mm). After surgery, at the time indicated in Table 1 (2 weeks for post 1 and 8 weeks for post 2 condition) another ophthalmologicalorthoptic examination was done for all children. At this time, the squint angle was reduced considerably for all children. Importantly, in post 1 condition three children (C2, C4 and C7) gained normal binocular vision and in the post 2 condition the child C3 also gained stereopsis. Children C2, C4 and C7 who in the post 1 condition showed stereopsis maintained or improved its level afterwards in the post 2 condition. A platform (principle of strain gauge) consisting of two dynamometric clogs (standards by Association Franc¸aise de Posturologie, produced by TechnoConcept, Céreste, France) was used to measure postural stability. Excursions of center of pressure (CoP) were recorded during 25.6 s. The platform posturography is equipped with an analog–digital (16 bit) and the acquisition frequency is 40 Hz. The visual stimuli were presented on a flat screen (1280 × 768 pixels), placed 80 cm from the children. The elevation of the screen was adjusted as a function of the height of each child in order that its center was facing exactly the eyes. Two of the five components of optical flow were used as visual stimuli: the contraction (C) and the expansion (E). Each was realized by clouds of bright points (brightness 50 cd/m2 ; number 50; diameter 0.235; density 0.44 point/deg2 ) appearing on a black background in a circular window of 12◦ of diameter, with a blind zone in the center of a diameter of 0.7◦ , and a speed of movement of 5.6◦ /s. The position of points from the stimulation was random [10]. The child was standing on the platform, in front of the screen located 80 cm away from him/her. Postural measurements were performed in two different conditions: with eyes open (EO) and with both eyes closed (EC). The order of the two conditions varied randomly between the children. Each test was followed by a rest lasting for a few minutes. The child was instructed to stay as stable as possible, with the arms along the body. To quantify the postural performances from data obtained from the platform, we analysed the surface and the variance of speed of the CoP excursion. Indeed, the surface area is a good measure of CoP spatial variability [27] and the variance of speed represents a good index of the amount of neuromuscular activity required to regulate postural control [8]. In addition, the spent energy was evaluated (in percentage) on the basis of the total frequency of the body oscillations. For that, the frequency spectrum of the platform oscillations was calculated from 0 to 20 Hz by fast Fourier transformation and it was divided into three frequency bands: low frequency, 0–0.5 Hz; medium frequency, 0.50–2 Hz; high frequency, >2 Hz. This latter analysis has enabled assessment of the preferential involvement of short or long neuronal loops in balance regulation. In agreement with other authors, we assumed that:
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Table 1 Clinical characteristics of children. Glasses correction
C1 (4) C2 (4) C3 (4) C4 (7) C5 (7) C6 (7) C7 (8) C8 (8) C9 (8)
RE + 4.25(−1.25 × 165) LE + 5(−1.5 × 0) RE + 0.75(−0.25 × 160) LE + 0.5 RE + 3.5(−1 × 175) LE + 3.5(−1 × 35) RE + 1 LE + 1.25 RE + 6(−1.75 × 154) LE + 7(−2 × 45) RE + 2.5(−1.25 × 10) LE + 3(−1 × 160) RE + 3.5(−0.75 × 180) LE + 4.5(−0.75 × 165) RE + 4.25(−0.25 × 100) LE + 3.75(−0.75 × 65) RE + 5.75 LE + 6.00
Pre surgery
Post 1 surgery
Corrected visual acuity
Dominant eye
Angle of strabismus (prism D)
Stereo acuity (TNO test)
Type of surgical treatment
Angle of strabismus (prism D)
10/10 10/10 10/10 10/10 10/10 10/10 10/10 10/10 10/10 10/10 9/10 9/10 10/10 10/10 9/10 10/10 10/10 10/10
RE
ET20 E T35 XT40 X T45 ET30 E T35 XT45 X X T18 ET50 E T50 ET18 E T18 ET20 E T30 ET35 E T35 ET25 E T35
–
a, c RE, LE
–
b, d RE
–
a, e LE
–
b, d LE
–
a, e RE
–
a, e RE
ET6 E T16 XT6 E T6 XT30 X T20 E4 O ET35 E T35 ET8 E E T2 E2 E 2 ET14 E T16 XT16 X T14
LE RE RE LE RE LE LE RE
–
a, c RE, LE
–
a, e RE
–
a RE, LE
Post 2 surgery Stereo acuity (TNO test)
80 – 50 – –
140 – –
Angle of strabismus (prism D)
Stereo acuity (TNO test)
XT8 E T4 XT10 E E T10 XT10 X T14 X2 O ET12 E T25 XXT4 X X T6 O O ET8 E T10 XT4 X T8
– 80 400 50 – – 60 – –
LE, RE, left eye, right eye; all children had good visual acuity for both eyes. The dominant eye was determined by using the 4 prism D base-out prism test: the prism was alternated over the left and the right eye; the eye for which the prism caused more frequently a refixation movement was considered as dominant. The deviation of the eyes was assessed with several tests (e.g. cover–uncover test, prism, and synoptophore); the binocular vision was evaluated with the TNO test for stereoscopic depth discrimination. XT–XXT = exophoria–exotropia deviation measured at far distance (5 m), X T–X X T = exophoria–exotropia deviation measured at near distance (30 cm), ET–EET = esophoria–esotropia deviation measured at far distance (5 m), E T–E E T = esophoria–esotropia deviation measured at near distance (30 cm). O and O = orthophoria measured at far (5 m) and at near (30 cm) distance, respectively. Type of surgical treatment: a = medial rectus resection; b = lateral rectus resection; c = Cüppers technique (Faden procedure); d = medial rectus resection or tightening; e = lateral rectus resection or tightening.
A. Legrand et al. / Neuroscience Letters 501 (2011) 96–101
Children (years)
A. Legrand et al. / Neuroscience Letters 501 (2011) 96–101
(A)
Surface of the CoP (mm2)
700 600 500
pre
400
post 1
300
post 2
200 100 0 C EO
(B)
C EC
E EO
E EC
Variance of speed (mm2/s2)
700 600 500 400 300 200 100 0 C EO
C EC
E EO
E EC
Fig. 1. Means and standard deviations for surface (A) and variance of speed (B) of CoP for all children examined before (pre) and two times after surgery (post 1 and post 2) with the two different stimulations (contraction, C and expansion, E) and in the two conditions (eye open, EO and eye closed, EC).
low frequencies account for visuovestibular regulation (long loop regulation); medium frequencies account for cerebellar participation, and high frequencies account for proprioceptive participation (myotatic loop) [20]. Analysis of variance (using the ANOVA test) was performed to compare postural data in the different visual conditions (eyes open or eyes closed) with the different type of stimulation (contraction and expansion) in the three experimental conditions (pre, post 1 and post 2). The effect of a factor was considered as significant when the p-value was below 0.05. For the frequency analysis the direction of the oscillations (along the medio-lateral axis and antero-posterior axis) was also taken in account. In Fig. 1 is reported the postural parameters (surface and variance of speed of the CoP) that were measured during the three experimental conditions: before (pre), 2 weeks (post 1) and 2 months (post 2) after surgery, while using contraction and expansion (C and E) as visual stimulations, with both eyes being kept open or closed (EO and EC respectively). Concerning the surface of the CoP (Fig. 1A), ANOVA test showed a significant effect of the surgery (F(2, 16) = 3.54, p < .05). In all cases, it was larger in the post 1 condition than in the pre condition, but then it decreased in the post 2 condition. ANOVA test showed also a significant effect of vision on the surface of CoP. The surface of the CoP was systematically smaller in the condition eyes open than in the condition eyes closed (F(1, 8) = 13.00, p < .007). With vision, such surface in the post 2 condition was even smaller than before surgery (pre condition), indicating that surgery was beneficial to postural stability. There was no effect of visual stimulation. Fig. 1B shows data obtained concerning the variance of speed of the CoP. Vision only had a significant effect (F(1, 8) = 24.81, p < .001): similar to the surface of the CoP, it was smaller in the condition eyes open than in the condition eyes closed. There were two additional interesting tendencies. First, except in one case (CEO), variance of speed had a tendency to increase immediately after surgery and then to decrease. Also, in the eyes open condition, variance of speed was systematically lower in the post 2 condition than in the pre con-
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dition. This was similar to what that was observed for the surface of CoP. In Fig. 2 is shown the frequencies of the body sways measured during the three experimental conditions: before (pre) and after (post 1 and post 2) surgery, using contraction and expansion as visual stimuli, in the two visual conditions (eyes open and eyes closed). For the low frequency body sways (Fig. 2A), ANOVA test showed a significant effect of the direction (F(1, 8) = 10.74, p < .01). The body sways in the antero-posterior direction were systematically larger compared to the body sways in the medio-lateral direction. In addition, there was a significant interaction between vision and direction but this was observed for the medio-lateral direction of body sways only (F(1, 8) = 25.97, p < .0001). In that case, the sway frequency power was significantly larger in the condition eyes open than in the condition eyes closed. Neither the surgery nor the type of visual stimulation modified these data. For the medium frequency body sways (Fig. 2B), ANOVA revealed a significant effect of the direction of sways (F(1, 8) = 9.35, p < .01). The body sways in the medio-lateral direction was larger than body sways in the antero-posterior direction. In addition, there was a significant interaction between vision and direction, concerning the medio-lateral body sways as well (F(1, 8) = 10.94, p < .01): the sway frequency power was significantly lower in the condition eyes open than in the condition eyes closed. Again, data did not seem to depend on the surgery or the type of visual stimulation. Finally, for the high frequency body sways (Fig. 2C), the ANOVA showed a significant effect of the surgery (F(2, 16) = 4.30, p < .03) but only in case of the medio-lateral body sways: in the post 2 condition, the body sways were larger compared to pre and post 1 condition. There was also a significant effect of the direction (F(1, 9) = 13.07, p < .006) meaning that the body sways in the medio-lateral direction was larger with respect to that of the antero-posterior direction. The goal of the study was to explore postural capabilities in children with strabismus before and after strabismus surgery. The main findings reported in the present study are as follows: (i) significant effects of eye surgery on the surface of the CoP and on the high-frequency band; (ii) significant effect of vision on the surface and variance of speed of the CoP and also on the high and medium-frequency bands. These findings will be discussed individually below. The effect of surgery on postural stability is different depending on the delay of the measures performed. In the post 1 condition (about 2 weeks after surgery) postural control is low and both the surface of the CoP and the variance of speed increased with respect to the pre surgery condition. This occurs in both conditions with eyes open as well as eyes closed. This finding is in agreement with the study of Matsuo et al. [14] showing that 3 days after strabismus surgery body sway increased considerably in strabismic children. According to these results we suggest that visual input is not the only one affected. As showed by Buisseret [6] extra-ocular muscles have several proprioceptive receptors providing information about the position of the eye in its orbit. Most likely, proprioceptive inputs associated with extra-ocular muscles are also influenced by surgery. Indeed, it is well known that eye surgery alters the proprioceptive information of the derived eye [24]. Interesting, the second postural measure done about 8 weeks after strabismus surgery reported an improvement in postural control. This finding is new. We make the hypothesis that tissue healing after 8 weeks is almost completed and the realignment of the visual axis facilitates visual perception [24] leading to better postural stability. Finally analysis of high frequency provided some new findings: in the post 2 surgery condition, the energy expended by the
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A. Legrand et al. / Neuroscience Letters 501 (2011) 96–101
Medio-Lateral
(A)
%
Low frequency
90
90
80
80
70
70
60
60
50
50
40
40
30
30
20
20
10
10
0
0
C EO
(B)
Antero-Posterior
C EC
E EO
E EC
C EC
E EO
E EC
C EO
C EC
E EO
E EC
Medium frequency
% 40
40
35
35
30
30
25
25
20
20
15
15
10
10
5
5 0
0 C EO
(C)
C EO
C EC
E EO
E EC
High frequency
% 35
35
30
30
25
25
20
20
15
15
10
10
5
5
0
pre post 1 post 2
0
C EO
C EC
E EO
E EC
C EO
C EC
E EO
E EC
Fig. 2. Spectral energy at different frequency bands in the medio-lateral and antero-posterior directions with the two different stimulations (contraction, C and expansion, E) and in the two conditions (eye open, EO and eye closed, EC) measured before (pre) and two times after surgery (post 1 and post 2).
high frequency band in the medio-lateral is very high, suggesting an increase in muscular effort (myotatic loop) to control posture, according to the classification of Paillard et al. [20]. An important result of our study is that postural stability in strabismic children is globally better in the condition eyes open than in the condition eyes closed, both before and after surgery. This is similar to what is observed in typically developing children. These findings extend prior observations showing that children are more visuo dependent than adults [16]. Even though strabismic children have a deviated eye and no binocular vision (as was, at least, the case for all children in the pre condition), they use visual information to control their postural stability. This finding apparently contradicts previous work in children from Marucchi and Gagey [13] showing no difference in
postural control under eyes open and eyes closed conditions. On the other hand, it agrees with a more recent study of Matsuo et al. [14] reporting an improvement in the postural control with eyes open. Most likely, these different results could be due to the use of different methodologies. We suggest that, as adult subjects, strabismic children could use vestibular, proprioceptive and cerebellar processes to compensate for their visual impairment to assure good postural control [4,7,21,23]. The absence of any effect of visual stimulation on postural stability for strabismic children, observed here, could be due to a deficit in perceiving the two components of optical flow most tested. This could be due to the impaired vergence eye movements performances already reported in strabismic subjects [5]. Note however, that in this study we only tested two components of the
A. Legrand et al. / Neuroscience Letters 501 (2011) 96–101
optic flow (contraction and expansion), Further studies examining all components of optic flow combining eye movement recordings and postural measures are needed to further explore such issues. Finally, we should like to point out that our group of children was rather small and also heterogenous, by including different types of strabismus, with different refractive corrections and different binocular visual capabilities. We are aware that further postural examinations will need to be performed in the future on more subjects, displaying specifically one of the above mentioned ocular pathologies. This will allow to know more about the characteristics of each type of strabismus. Note however, that a recent report from Matsuo et al. [15] did not find any postural difference between adult with intermittent and congenital exotropia. In conclusion, this report shows that strabismus surgery affects temporarily postural stability in children. It remains unknown whether or not such effect persists in these children. Sensory adaptation changes observed particularly for the high frequency band could reach normal values via adaptive mechanisms that can occur after longer surgery to test interval. We conclude that postural measures and analysis of frequency is an interesting tool to further examine motor and sensory adaptations in children with strabismus. Acknowledgments The authors thank the children who participated in the study and Ms. Florence Groffal for the management of children’s appointments. They also thank Dr. Susan Sara for useful comments on the manuscript and englich corrections. References [1] A. Assaiante, S. Mallau, S. Viel, M. Jover, C. Schmitz, Development of postural control in healthy children: a functional approach , Neural Plasticity 12 (2005) 1–2. [2] Y. Blanchard, S. Carey, J. Coffey, A. Cohen, T. Harris, S. Michlik, G.L. Pellecchia, The influence of concurrent cognitive tasks on postural sway in children , Pediatr. Phys. Ther. 17 (3) (2005) 189–193. [3] T. Brandt, Vertigo, its Multisensory Syndromes , 2nd ed., Springer, 2003. [4] A.M. Bronstein, J.D. Hood, M.A. Gresty, C. Panagi, Visual control of balance in cerebellar and Parkinsonian syndromes , Brain 113 (3) (1990) 767–779. [5] M.P. Bucci, D. Brémond-Gignac, Z. Kapoula, Speed and accuracy of saccades, vergence and combined eye movements in subjects with strabismus before and after eye surgery , Vision Res. 49 (4) (2009) 460–469. [6] P. Buisseret, Influence of extraocular muscles proprioception on vision , Physiol. Rev. 75 (1995) 323–338.
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[7] M. Friedrich, H.J. Grein, C. Wicher, J. Schuetze, A. Mueller, A. Laurenroth, K. Hottenrott, R. Schwesig, Influence of pathologic and simulated visual dysfunctions on the postural system , Exp. Brain Res. 186 (2) (2008) 305–314. [8] A.C. Geurts, B. Nienhuis, T.W. Mulder, Intrasubject variability of selected forceplatform parameters in the quantification of postural control , Arch. Phys. Med. Rehabil. 74 (1993) 1144–1150. [9] G. Halmagyi, I. Curthoys, A clinical sign of canal paresis , Arch. Neurol. 45 (7) (1988) 737–739. [10] R.F. Hess, C.V. Hutchinson, T. Ledgeway, B. Mansouri, Binocular influences on global motion processing in the human visual system , Vision Res. 47 (2007) 1682–1692. [11] R.F. Hess, B. Mansouri, B. Thompson, Gheorghiu, Latent stereopsis for motion in depth in strabismic amblyopia , Invest. Ophthalmol. Vis. Sci. 50 (2009) 5006–5016. [12] C.S. Ho, D.E. Giaschi, Low- and high-level motion perception deficits in anisometropic and strabismic amblyopia: evidence from fMRI , Vision Res. 49 (2009) 2891–2901. [13] C. Marucchi, P.M. Gagey, Postural blindness , Agressologie 28 (9) (1987) 947–948. [14] T. Matsuo, A. Narita, M. Senda, S. Hasebe, H. Ohtsuki, Body sway increase immediately after strabismus surgery , Acta Med. Okayama 60 (2006) 13–24. [15] T. Matsuo, A. Yabuki, K. Hasebe, Y.H. Shira, S. Imai, H. Ohtsuki, Postural stability changes during the prism adaptation test in patients with intermittent and constant exotropia , Invest. Ophthalmol. Vis. Sci. 51 (12) (2010) 6341–6347. [16] V. Nougier, Contribution of central and peripheral vision to the regulation of stance: developmental aspects , J. Exp. Child Psychol. 68 (1998) 202–215. [17] P. Odenrick, P. Sandstedt, G. Lennerstrand, Postural sway and gait of children with convergent strabismus , Dev. Med. Child Neurol. 26 (4) (1984) 495–499. [18] I. Olivier, E. Palluel, V. Nougier, Effects of attentional focus on postural sway in children and adults , Exp. Brain Res. 185 (2008) 341–345. [19] I. Olivier, R. Cuisinier, M. Vaugoyeau, V. Nougier, C. Assaiante, Age-related differences in cognitive and postural dual-task performance , Gait Posture 32 (4) (2010) 494–499. [20] T. Paillard, C. Costes-Salon, C. Lafont, P. Dupui, Are there differences in postural regulation according to the level of competition in judoists? Br. J. Sports Med. 36 (2002) 304–305. [21] E. Ravaioli, S.K. Oie, T. Kiemel, L. Chiari, J. Jeka, Non linear postural control in response to visual translation , Exp. Brain Res. 160 (2005) 450–459. [22] A. Shumway-Cook, M.H. Woollacott, The growth of stability: postural control from a developmental perspective , J. Motor Bebav. 17 (1985) 131–147. [23] P. Sparto, M. Redfern, J. Jasko, M. Casselbrant, E. Mandel, J. Furman, The influence of dynamic visual cues for postural control in children aged 7–12 years , Exp. Brain Res. 168 (2006) 505–516. [24] M.J. Steinbach, D.R. Smith, Spatial localization after strabismus surgery: evidence for inflow , Science 213 (4514) (1981) 1407–1409. [25] R. Steindl, K. Kunz, A. Schrott-Fischer, A. Scholtz, Effect of age and sex on maturation of sensory systems and balance control , Dev. Med. Child Neurol. 48 (2006) 477–482. [26] G.K. Von Noorden, E.C. Campos, Binocular Vision and Ocular Motility. Theory and Management of Strabismus , 6th ed., Mosby, 2006. [27] N. Vuillerme, O. Chenu, N. Pinsault, A. Fleury, J. Demongeot, Y. Payan, Can a plantar pressure-based tongue-placed electrotactile biofeedback improve postural control under altered vestibular and neck proprioceptive conditions? Neuroscience 155 (2008) 291–296. [28] C.R. Weir, M. Cleary, S. Parks, T. Barrie, H.M. Hammer, J. Murdoch, Spatial localization after different types of retinal detachment surgery , Invest. Ophthalmol. Vis. Sci. 42 (7) (2001) 1495–1498.
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Neuroscience Letters journal homepage: www.elsevier.com/locate/neulet
Postural control in children with strabismus: Effect of eye surgery Agathe Legrand a,∗ , Emmanuel Bui Quoc b,c , Sylvette Wiener Vacher d , Jérôme Ribot c , Nicolas Lebas c , Chantal Milleret c , Maria Pia Bucci a a
Laboratoire de Psychologie et Neuropsychologie Cognitives, FRE 3292 CNRS IUPDP Université Paris Descartes, 71 Avenue Edouard Vaillant, 92774 Boulogne Billancourt Cedex, France Ophthalmology Department, Hôpital Robert Debré, 48 Boulevard Sérurier, 75019 Paris, France Laboratoire de Physiologie de la Perception et de l’Action, Collège de France, CNRS UMR 7152, 11 place Marcelin Berthelot, 75005 Paris, France d Ear Nose Throat and Cervico Facial Surgery Department, Hôpital Robert Debré, 48 Boulevard Sérurier, 75019 Paris, France b c
a r t i c l e
i n f o
Article history: Received 22 April 2011 Received in revised form 8 June 2011 Accepted 30 June 2011 Keywords: Children Strabismus Eye surgery Postural stability
a b s t r a c t The purpose of this study was to examine the postural control in children with strabismus before and after eye surgery. Control of posture is a complex multi-sensorial process relying on visual, vestibular and proprioceptive systems. Reduced influence of one of such systems leads to postural adaptation due to a compensation of one of the other systems [3]. Nine children with strabismus (4–8 years old) participated in the study. Ophthalmologic, orthoptic, vestibular and postural tests were done before and twice (2 and 8 weeks) after eye surgery. Postural stability was measured by a platform (TechnoConcept): two components of the optic flux were used for stimulation (contraction and expansion) and two conditions were tested eyes open and eyes closed. The surface area of the center of pressure (CoP), the variance of speed of the CoP and the frequency spectrum of the platform oscillations by fast Fourier transformation were analysed. Before surgery, similar to typically developing children, postural stability was better in the eyes open condition. The frequency analysis revealed that for the low frequency band more energy was spent in the antero-posterior direction compared to the medio-lateral one while the opposite occurred for the middle and the high frequency bands. After surgery, the eye deviation was reduced in all children and their postural stability also improved. However, the energy of the high frequency band in the mediolateral direction increased significantly. These findings suggest that eye surgery influences somatosensory properties of extra-ocular muscles leading to improvement of postural control and that binocular visual perception could influence the whole body. © 2011 Elsevier Ireland Ltd. All rights reserved.
Posture involves a coordinated relationship of the different segments of the body. It promotes balance, which is the ability to maintain a stable condition at any time. Control of posture is a complex process based on multiple interactions among visual, vestibular and proprioceptive sensory systems. Reducing the influence of one system leads to postural adaptation due to a compensation by one of the other systems [3]. As described by Assaiante et al. [1], the development of postural control takes place during the growth of the child. The child builds a repertoire of postural strategies. Subsequently, he must learn to choose the best strategy in a situation of imbalance. By examining postural stability in 140 children aged 3–16 years, Steindl et al. [25] suggested that a child only reaches postural maturation at about 10 years of age. There is therefore a strong interaction between postural control and age (but no gender difference). Postural control has long been regarded as an automatic response. But recent studies have shown the existence of a pos-
∗ Corresponding author. E-mail address: [email protected] (A. Legrand). 0304-3940/$ – see front matter © 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.neulet.2011.06.056
ture regulation process, both in case of a simple task or a more complicated one, involving several attention processes [2]. The mobilization of such attentional sources is dependent on many factors such as the age, availability of sensory information, the complexity of the task and postural skills. In this regard, Olivier et al. [18,19] showed an effect of attention on body sway depending on age. From their data, they suggested that the mature level of attention was not reached before 11 years old. Furthermore, it appeared that both children and adults had to concentrate their attention and to spend energy to reach good postural stability. Quantifications of postural stability on a fixed or a movable surface in 7–12 year old children revealed an increase of body sway in case of a moving surface [23]. Similarly, in a dynamically moving scene, for example, after presentation of a stimulus reproducing optical flow (by alternating concentric circles of black and white or black and white squares), the maintenance of standing in children was shown to be more difficult than in the adult. This was due to the involvement of two conflicting sensory inputs: some visual and some vestibular. They emphasized that the conflict of sensory inputs is difficult to manage for the young child. This is strengthened by the fact that children are particularly visually dependent
A. Legrand et al. / Neuroscience Letters 501 (2011) 96–101
(more than the adults are). Indeed, it is well known that vision plays a major role in postural control in children: to closure their eyes greatly impairs balance. This indicates that visual information is one of the most important sources for postural stabilization [22]. As a consequence, a dysfunction of visual input in children might induce difficulties in maintaining proper postural balance. But surprisingly this has been as yet only poorly investigated. In about 4% of young population sensory and/or motor pathways are not correctly developed leading to a misalignment of the visual axis and strabismus. Strabismus eye surgery is one of the methods used for treatment [26]. Studies examining the relationship between strabismus and posture are very scarce. From our knowledge at least, there are only two. First, more than twenty years ago, a Swedish study reported that the presence of exotropia was accompanied by greater body sways [17]. Second, more recently, a study was conducted in Japan [14] on postural balance in strabismic children from 3 to 12 years before and after surgery. These authors reported greater postural instability after strabismus surgery than before, whether the eyes were kept open or closed. Importantly, children with binocular capabilities were more stable after surgery than children having no stereopsis. Unfortunately, data obtained before surgery in the conditions eyes open and eyes closed were not compared each other. Another important point may be critical. Posture was recorded 3 days after surgery while anesthetic may still have some effects on the body, and therefore on the proprioception of extraocular muscles [28]. In the present study, we examined the quality of postural control before and after strabismus surgery. After surgery, performances were compared after two different postsurgery delays: 2 weeks and 2 months. Posture was quantified while children were looking at some components of the optic flow (contraction vs. expansion). Our choice was guided by the fact that perception of movement is known to be impaired in strabismic amblyopic subjects only [11,12]. In accordance with Matsuo et al. [14], we expected to find poor postural control, at least in the post 1 surgery condition, because of the proprioceptive changes in the extra-ocular muscles [6]. In the post 2 surgery condition, stability of children could be improved via adaptive mechanisms. Nine strabismic children between 4 and 8 years old participated in the study. The investigation adhered to the principles of the Declaration of Helsinki and was approved by our institutional Human Experimentation Committee. Informed parental consent was obtained for each subject after the nature of the procedure had been explained. Prior to surgey all children underwent a complete ophthalmological, orthoptic and vestibular examination. Global vestibular and proprioception evaluation was done using two clinical tests: the Romberg eye open and closed and the Halmagyi tests or head thrust test. The Romberg test is performed by asking the child to stand, feet close to each other and arms along the trunk with eyes open and eyes closed, on a hard surface and a soft surface (mattress). The child was asked to stand quietly in this position for 20 s with a minimal sway. The Head thrust test [9] evaluates the function of the semicircular canals of the vestibular receptors. The head is rotated passively and briefly on the planes of a semicircular canals while the child is asked to fixate a target placed at 60 cm from him. A right horizontal head rotation evaluates the function of the right semicircular canal, to the left for the left horizontal canal. The eyes can stay on the target in such a rapid head movement only if the canal tested is functional. If the canal is not functional the eyes are first moving with the head during the head rotation and then making a rapid saccade to bring back the gaze on the target: this catch up saccade indicates a deficit of the corresponding canal. A normal clinical Halmagyi test without catch up saccade indicates a normal vestibular canal func-
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tion. In our study all children had a normal Romberg and Halmagyi test. Clinical data of each child are shown in Table 1. Seven children (C1, C3, C5, C6, C7, C8 and C9) had convergent strabismus (esotropia): more precisely, four of them (C3, C5, C6 and C8) had infantile esotropia, two children (C1 and C7) had partially accommodative esotropia and one child only (C9) had secondary esotropia. The other two children (C2 and C4) had divergent strabismus (exotropia). Binocular visual capability was assessed with the TNO test and no child showed stereopsis. All children underwent strabismus surgery. Two children (C1 and C7) underwent bilateral medial rectus recession (3–4 mm) combined with the Cüppers technique; one child (C9) underwent bilateral medial rectus recession (8 mm); four children (C3, C5, C6 and C8) underwent medial rectus recession (4–7 mm) combined with lateral rectus resection (4–7 mm) and two children (C2 and C4) underwent lateral rectus recession (6 mm) combined with medial rectus resection (7 mm). After surgery, at the time indicated in Table 1 (2 weeks for post 1 and 8 weeks for post 2 condition) another ophthalmologicalorthoptic examination was done for all children. At this time, the squint angle was reduced considerably for all children. Importantly, in post 1 condition three children (C2, C4 and C7) gained normal binocular vision and in the post 2 condition the child C3 also gained stereopsis. Children C2, C4 and C7 who in the post 1 condition showed stereopsis maintained or improved its level afterwards in the post 2 condition. A platform (principle of strain gauge) consisting of two dynamometric clogs (standards by Association Franc¸aise de Posturologie, produced by TechnoConcept, Céreste, France) was used to measure postural stability. Excursions of center of pressure (CoP) were recorded during 25.6 s. The platform posturography is equipped with an analog–digital (16 bit) and the acquisition frequency is 40 Hz. The visual stimuli were presented on a flat screen (1280 × 768 pixels), placed 80 cm from the children. The elevation of the screen was adjusted as a function of the height of each child in order that its center was facing exactly the eyes. Two of the five components of optical flow were used as visual stimuli: the contraction (C) and the expansion (E). Each was realized by clouds of bright points (brightness 50 cd/m2 ; number 50; diameter 0.235; density 0.44 point/deg2 ) appearing on a black background in a circular window of 12◦ of diameter, with a blind zone in the center of a diameter of 0.7◦ , and a speed of movement of 5.6◦ /s. The position of points from the stimulation was random [10]. The child was standing on the platform, in front of the screen located 80 cm away from him/her. Postural measurements were performed in two different conditions: with eyes open (EO) and with both eyes closed (EC). The order of the two conditions varied randomly between the children. Each test was followed by a rest lasting for a few minutes. The child was instructed to stay as stable as possible, with the arms along the body. To quantify the postural performances from data obtained from the platform, we analysed the surface and the variance of speed of the CoP excursion. Indeed, the surface area is a good measure of CoP spatial variability [27] and the variance of speed represents a good index of the amount of neuromuscular activity required to regulate postural control [8]. In addition, the spent energy was evaluated (in percentage) on the basis of the total frequency of the body oscillations. For that, the frequency spectrum of the platform oscillations was calculated from 0 to 20 Hz by fast Fourier transformation and it was divided into three frequency bands: low frequency, 0–0.5 Hz; medium frequency, 0.50–2 Hz; high frequency, >2 Hz. This latter analysis has enabled assessment of the preferential involvement of short or long neuronal loops in balance regulation. In agreement with other authors, we assumed that:
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Table 1 Clinical characteristics of children. Glasses correction
C1 (4) C2 (4) C3 (4) C4 (7) C5 (7) C6 (7) C7 (8) C8 (8) C9 (8)
RE + 4.25(−1.25 × 165) LE + 5(−1.5 × 0) RE + 0.75(−0.25 × 160) LE + 0.5 RE + 3.5(−1 × 175) LE + 3.5(−1 × 35) RE + 1 LE + 1.25 RE + 6(−1.75 × 154) LE + 7(−2 × 45) RE + 2.5(−1.25 × 10) LE + 3(−1 × 160) RE + 3.5(−0.75 × 180) LE + 4.5(−0.75 × 165) RE + 4.25(−0.25 × 100) LE + 3.75(−0.75 × 65) RE + 5.75 LE + 6.00
Pre surgery
Post 1 surgery
Corrected visual acuity
Dominant eye
Angle of strabismus (prism D)
Stereo acuity (TNO test)
Type of surgical treatment
Angle of strabismus (prism D)
10/10 10/10 10/10 10/10 10/10 10/10 10/10 10/10 10/10 10/10 9/10 9/10 10/10 10/10 9/10 10/10 10/10 10/10
RE
ET20 E T35 XT40 X T45 ET30 E T35 XT45 X X T18 ET50 E T50 ET18 E T18 ET20 E T30 ET35 E T35 ET25 E T35
–
a, c RE, LE
–
b, d RE
–
a, e LE
–
b, d LE
–
a, e RE
–
a, e RE
ET6 E T16 XT6 E T6 XT30 X T20 E4 O ET35 E T35 ET8 E E T2 E2 E 2 ET14 E T16 XT16 X T14
LE RE RE LE RE LE LE RE
–
a, c RE, LE
–
a, e RE
–
a RE, LE
Post 2 surgery Stereo acuity (TNO test)
80 – 50 – –
140 – –
Angle of strabismus (prism D)
Stereo acuity (TNO test)
XT8 E T4 XT10 E E T10 XT10 X T14 X2 O ET12 E T25 XXT4 X X T6 O O ET8 E T10 XT4 X T8
– 80 400 50 – – 60 – –
LE, RE, left eye, right eye; all children had good visual acuity for both eyes. The dominant eye was determined by using the 4 prism D base-out prism test: the prism was alternated over the left and the right eye; the eye for which the prism caused more frequently a refixation movement was considered as dominant. The deviation of the eyes was assessed with several tests (e.g. cover–uncover test, prism, and synoptophore); the binocular vision was evaluated with the TNO test for stereoscopic depth discrimination. XT–XXT = exophoria–exotropia deviation measured at far distance (5 m), X T–X X T = exophoria–exotropia deviation measured at near distance (30 cm), ET–EET = esophoria–esotropia deviation measured at far distance (5 m), E T–E E T = esophoria–esotropia deviation measured at near distance (30 cm). O and O = orthophoria measured at far (5 m) and at near (30 cm) distance, respectively. Type of surgical treatment: a = medial rectus resection; b = lateral rectus resection; c = Cüppers technique (Faden procedure); d = medial rectus resection or tightening; e = lateral rectus resection or tightening.
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Surface of the CoP (mm2)
700 600 500
pre
400
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300
post 2
200 100 0 C EO
(B)
C EC
E EO
E EC
Variance of speed (mm2/s2)
700 600 500 400 300 200 100 0 C EO
C EC
E EO
E EC
Fig. 1. Means and standard deviations for surface (A) and variance of speed (B) of CoP for all children examined before (pre) and two times after surgery (post 1 and post 2) with the two different stimulations (contraction, C and expansion, E) and in the two conditions (eye open, EO and eye closed, EC).
low frequencies account for visuovestibular regulation (long loop regulation); medium frequencies account for cerebellar participation, and high frequencies account for proprioceptive participation (myotatic loop) [20]. Analysis of variance (using the ANOVA test) was performed to compare postural data in the different visual conditions (eyes open or eyes closed) with the different type of stimulation (contraction and expansion) in the three experimental conditions (pre, post 1 and post 2). The effect of a factor was considered as significant when the p-value was below 0.05. For the frequency analysis the direction of the oscillations (along the medio-lateral axis and antero-posterior axis) was also taken in account. In Fig. 1 is reported the postural parameters (surface and variance of speed of the CoP) that were measured during the three experimental conditions: before (pre), 2 weeks (post 1) and 2 months (post 2) after surgery, while using contraction and expansion (C and E) as visual stimulations, with both eyes being kept open or closed (EO and EC respectively). Concerning the surface of the CoP (Fig. 1A), ANOVA test showed a significant effect of the surgery (F(2, 16) = 3.54, p < .05). In all cases, it was larger in the post 1 condition than in the pre condition, but then it decreased in the post 2 condition. ANOVA test showed also a significant effect of vision on the surface of CoP. The surface of the CoP was systematically smaller in the condition eyes open than in the condition eyes closed (F(1, 8) = 13.00, p < .007). With vision, such surface in the post 2 condition was even smaller than before surgery (pre condition), indicating that surgery was beneficial to postural stability. There was no effect of visual stimulation. Fig. 1B shows data obtained concerning the variance of speed of the CoP. Vision only had a significant effect (F(1, 8) = 24.81, p < .001): similar to the surface of the CoP, it was smaller in the condition eyes open than in the condition eyes closed. There were two additional interesting tendencies. First, except in one case (CEO), variance of speed had a tendency to increase immediately after surgery and then to decrease. Also, in the eyes open condition, variance of speed was systematically lower in the post 2 condition than in the pre con-
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dition. This was similar to what that was observed for the surface of CoP. In Fig. 2 is shown the frequencies of the body sways measured during the three experimental conditions: before (pre) and after (post 1 and post 2) surgery, using contraction and expansion as visual stimuli, in the two visual conditions (eyes open and eyes closed). For the low frequency body sways (Fig. 2A), ANOVA test showed a significant effect of the direction (F(1, 8) = 10.74, p < .01). The body sways in the antero-posterior direction were systematically larger compared to the body sways in the medio-lateral direction. In addition, there was a significant interaction between vision and direction but this was observed for the medio-lateral direction of body sways only (F(1, 8) = 25.97, p < .0001). In that case, the sway frequency power was significantly larger in the condition eyes open than in the condition eyes closed. Neither the surgery nor the type of visual stimulation modified these data. For the medium frequency body sways (Fig. 2B), ANOVA revealed a significant effect of the direction of sways (F(1, 8) = 9.35, p < .01). The body sways in the medio-lateral direction was larger than body sways in the antero-posterior direction. In addition, there was a significant interaction between vision and direction, concerning the medio-lateral body sways as well (F(1, 8) = 10.94, p < .01): the sway frequency power was significantly lower in the condition eyes open than in the condition eyes closed. Again, data did not seem to depend on the surgery or the type of visual stimulation. Finally, for the high frequency body sways (Fig. 2C), the ANOVA showed a significant effect of the surgery (F(2, 16) = 4.30, p < .03) but only in case of the medio-lateral body sways: in the post 2 condition, the body sways were larger compared to pre and post 1 condition. There was also a significant effect of the direction (F(1, 9) = 13.07, p < .006) meaning that the body sways in the medio-lateral direction was larger with respect to that of the antero-posterior direction. The goal of the study was to explore postural capabilities in children with strabismus before and after strabismus surgery. The main findings reported in the present study are as follows: (i) significant effects of eye surgery on the surface of the CoP and on the high-frequency band; (ii) significant effect of vision on the surface and variance of speed of the CoP and also on the high and medium-frequency bands. These findings will be discussed individually below. The effect of surgery on postural stability is different depending on the delay of the measures performed. In the post 1 condition (about 2 weeks after surgery) postural control is low and both the surface of the CoP and the variance of speed increased with respect to the pre surgery condition. This occurs in both conditions with eyes open as well as eyes closed. This finding is in agreement with the study of Matsuo et al. [14] showing that 3 days after strabismus surgery body sway increased considerably in strabismic children. According to these results we suggest that visual input is not the only one affected. As showed by Buisseret [6] extra-ocular muscles have several proprioceptive receptors providing information about the position of the eye in its orbit. Most likely, proprioceptive inputs associated with extra-ocular muscles are also influenced by surgery. Indeed, it is well known that eye surgery alters the proprioceptive information of the derived eye [24]. Interesting, the second postural measure done about 8 weeks after strabismus surgery reported an improvement in postural control. This finding is new. We make the hypothesis that tissue healing after 8 weeks is almost completed and the realignment of the visual axis facilitates visual perception [24] leading to better postural stability. Finally analysis of high frequency provided some new findings: in the post 2 surgery condition, the energy expended by the
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Medio-Lateral
(A)
%
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Medium frequency
% 40
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10
5
5
0
pre post 1 post 2
0
C EO
C EC
E EO
E EC
C EO
C EC
E EO
E EC
Fig. 2. Spectral energy at different frequency bands in the medio-lateral and antero-posterior directions with the two different stimulations (contraction, C and expansion, E) and in the two conditions (eye open, EO and eye closed, EC) measured before (pre) and two times after surgery (post 1 and post 2).
high frequency band in the medio-lateral is very high, suggesting an increase in muscular effort (myotatic loop) to control posture, according to the classification of Paillard et al. [20]. An important result of our study is that postural stability in strabismic children is globally better in the condition eyes open than in the condition eyes closed, both before and after surgery. This is similar to what is observed in typically developing children. These findings extend prior observations showing that children are more visuo dependent than adults [16]. Even though strabismic children have a deviated eye and no binocular vision (as was, at least, the case for all children in the pre condition), they use visual information to control their postural stability. This finding apparently contradicts previous work in children from Marucchi and Gagey [13] showing no difference in
postural control under eyes open and eyes closed conditions. On the other hand, it agrees with a more recent study of Matsuo et al. [14] reporting an improvement in the postural control with eyes open. Most likely, these different results could be due to the use of different methodologies. We suggest that, as adult subjects, strabismic children could use vestibular, proprioceptive and cerebellar processes to compensate for their visual impairment to assure good postural control [4,7,21,23]. The absence of any effect of visual stimulation on postural stability for strabismic children, observed here, could be due to a deficit in perceiving the two components of optical flow most tested. This could be due to the impaired vergence eye movements performances already reported in strabismic subjects [5]. Note however, that in this study we only tested two components of the
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optic flow (contraction and expansion), Further studies examining all components of optic flow combining eye movement recordings and postural measures are needed to further explore such issues. Finally, we should like to point out that our group of children was rather small and also heterogenous, by including different types of strabismus, with different refractive corrections and different binocular visual capabilities. We are aware that further postural examinations will need to be performed in the future on more subjects, displaying specifically one of the above mentioned ocular pathologies. This will allow to know more about the characteristics of each type of strabismus. Note however, that a recent report from Matsuo et al. [15] did not find any postural difference between adult with intermittent and congenital exotropia. In conclusion, this report shows that strabismus surgery affects temporarily postural stability in children. It remains unknown whether or not such effect persists in these children. Sensory adaptation changes observed particularly for the high frequency band could reach normal values via adaptive mechanisms that can occur after longer surgery to test interval. We conclude that postural measures and analysis of frequency is an interesting tool to further examine motor and sensory adaptations in children with strabismus. Acknowledgments The authors thank the children who participated in the study and Ms. Florence Groffal for the management of children’s appointments. They also thank Dr. Susan Sara for useful comments on the manuscript and englich corrections. References [1] A. Assaiante, S. Mallau, S. Viel, M. Jover, C. Schmitz, Development of postural control in healthy children: a functional approach , Neural Plasticity 12 (2005) 1–2. [2] Y. Blanchard, S. Carey, J. Coffey, A. Cohen, T. Harris, S. Michlik, G.L. Pellecchia, The influence of concurrent cognitive tasks on postural sway in children , Pediatr. Phys. Ther. 17 (3) (2005) 189–193. [3] T. Brandt, Vertigo, its Multisensory Syndromes , 2nd ed., Springer, 2003. [4] A.M. Bronstein, J.D. Hood, M.A. Gresty, C. Panagi, Visual control of balance in cerebellar and Parkinsonian syndromes , Brain 113 (3) (1990) 767–779. [5] M.P. Bucci, D. Brémond-Gignac, Z. Kapoula, Speed and accuracy of saccades, vergence and combined eye movements in subjects with strabismus before and after eye surgery , Vision Res. 49 (4) (2009) 460–469. [6] P. Buisseret, Influence of extraocular muscles proprioception on vision , Physiol. Rev. 75 (1995) 323–338.
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