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Auris Nasus Larynx 31 (2004) 11–17 Monocular versus binocular vision in postural control Elina Isotalo a,b,∗ , Zoi Kapoula a,1 , Pierre-Henri Feret c , Karine Gauchon c , Françoise Zamfirescu c , Pierre-Marie Gagey d a LPPA, Collège de France CNRS, 11 place Marcelin Berthelot, 4 F-75005 Paris, France Department of Ear, Nose and Throat, Helsinki University Central Hospital, Haartmaninkatu 4E, FIN-00290 Hus, Finland Centre National Hospitalier d’Ophthalmologie des Quinze-Vingts, service du Pr. L. Laroche, 28 rue de Charenton, 755571 Paris, France d Institut de Posturologie, avenue de Carbéra, 75012 Paris, France b c Received 2 March 2003; accepted 14 October 2003 Abstract Objective: In previous studies about the control of posture there have been controversial findings. Our aim was to examine the role of monocular and binocular vision in controlling posture in quiet stance. Methods: Twenty-eight normal subjects were tested. We used a force platform in measuring postural stability. In main experiment, postural stability was measured in four conditions: both eyes open (BEO), dominant eye open (DEO) non-dominant eye open (NDEO), and both eyes closed (BEC). In a further experiment, 11 subjects were tested in conditions where a vertical prism was placed in front of dominant eye. Prism was strong enough to cause diplopia. Our interest was to see, if diplopia affected the balance. Results: In main experiment, at level of group the body-sway in any of the three ocular (viewing) conditions did not differ from each other. At level of individuals, binocular vision was more effective on controlling posture in only half of subjects. In prism experiment, relative to normal binocular viewing the postural stability was modified in both prism conditions, but there was no difference between monocular and binocular viewing with prism. Conclusion: In quiet stance and in subjects with perfect binocular vision and stereopsis, the benefit out of binocular viewing in postural stability is subject-dependent. At the level of group, monocular vision provides equally good postural stability as binocular vision. © 2003 Elsevier Ireland Ltd. All rights reserved. Keywords: Binocular vision; Monocular vision; Balance; Posturography 1. Introduction The visual system has been shown to be important in the postural control by means of comparing the area of body-sway with eyes open and eyes closed. It has been found that in normal subjects the sway area is 2–3 times larger with eyes closed than with eyes open [1–3]. Gentaz [4] studied the control of balance in 40 normal subjects with posturographic tests in monocular conditions where either dominant or non-dominant eye were covered. He suggested that there is a preferred eye, the so-called “postural eye” that allows better postural stability than the non-preferred eye, and that the postural eye is not necessarily the dominant eye [4]. ∗ Corresponding author. Tel.: +358-9-4711; fax: +358-9-4717-5010. E-mail addresses: [email protected] (E. Isotalo), [email protected] (Z. Kapoula). 1 Tel.: +33-1-44-27-16-35; fax: +33-1-44-27-13-82. In earlier studies, the patients with strabismus have been found to have reduced postural stability when compared with normal subjects, even though these patients can have normal visual acuity in each eye [5–7]. In binocular conditions, patients with strabismus can have diplopia. Ocular misalignment with diplopia or altered ocular proprioceptive signals could be the cause of reduced postural stability in these patients in visual conditions [7]. Fox [8] has studied, whether postural stability under visual conditions employs mainly monocular visual input or binocular visual input. He examined the effect of binocular and monocular (with dominant eye open) visual conditions and the non-visual condition on the postural control in a normal population. The postural stability was better under binocular vision than under monocular vision. This benefit, however, was found to be present even in dark, which was interpreted as evidence against the role of the binocular vision per se. We decided to study his hypothesis further. 0385-8146/$ – see front matter © 2003 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.anl.2003.10.001 12 E. Isotalo et al. / Auris Nasus Larynx 31 (2004) 11–17 Fox [8] also made an additional experiment about the effect of proprioceptive information (standard and tandem Romberg conditions) in the control of posture in binocular and monocular conditions in light. The standard Romberg was more stable than the tandem Romberg in different conditions. The tandem Romberg condition had little effect on body-sway in the binocular condition. But, in monocular condition the body-sway was increased. So, the binocular vision had a stabilizing effect. The tandem Romberg posture amplified the visual influence, since it attenuated the usefulness of proprioceptive input and reflexes on postural equilibrium. In a recent paper, Guerraz et al. [9] studied the effect of motion parallax and binocular versus monocular vision in the control of posture in eight subjects. They found that the effect of motion parallax on body-sway was of monocular origin. In their study, monocular viewing was studied only with the dominant eye, as in the study of Fox [8]. In a recent study of Kunkel et al. [10], the efficacy of visual stabilization of posture was investigated with different spatial frequencies of a visual stimulus. They found that none of the stimuli in monocular condition diminished the sway parameters as effectively as unrestricted binocular vision did. Thus, previous studies in normal subjects provide rather controversial answers to the question of the importance of monocular or binocular vision in controlling posture. However, the methods used have varied remarkably in those studies cited above. All of them bring some aspects related to the question of the role of binocular/monocular vision in the control of posture. The purpose of our study was to re-examine the role of monocular versus binocular vision in postural control. We extended the study by examining the monocular condition also with the non-dominant eye open in addition to the condition with dominant eye open. We designed a further experiment where we used a prism to test directly the effect of disruption of binocular vision on postural stability. 2. Subjects and methods 2.1. Subjects and preliminary tests Twenty-eight subjects participated in this study. All subjects were healthy without any neurological, otoneurological or ophthalmological symptoms. Informed consents according to the Helsinki Declaration were given. Preliminary examinations were done to all the subjects participating in the study. They included measures of visual acuity, binocular vision (TNO test for stereoacuity, Wirt and Lang tests), and fusional disparity-vergence (bar-prism test). Eye dominance was determined with subjective tests (pointing task, fixating via a hole task) and with the Jampolsky 4 prism-diopters test based on the observation of movements of the eyes, when the prism was placed or removed in front of each eye. Normality of the controlling of balance was eval- uated with the Unterberger/Fukuda stepping test. Eighteen out of the 28 subjects could be considered healthy according to the preliminary tests. Nine subjects had pathological findings in the preliminary examinations, particularly in the tests assessing the control of balance, and one subject had a disparity of 1 cm in the length of the legs. 2.2. Posturography We used a force platform (standards by Association Francaise de Posturologie (AFP) [11]; produced by Dynatronic, Céreste, France) to measure the postural stability (principle of strain gauge; [11]). The alteration of center point of force (CFP) was measured during a 50 s period. The equipment contained also an AD converter of 12 bits. Resolution of the measures was 0.001 m, and the frequency response of the platform was more than 10 times the highest frequency studied (the exact frequency response was not assessed). The parameter analyzed in each condition was the surface area of CFPs [12]. CFP and its changes were assessed by the force platform during the testing with the sampling frequency of 5 Hz, and after the test the recorded results were converted to the surface area of CFPs [12]. The surface area of the CFPs was assessed so that 90% of the CFPs were inside an ellipsoid [12]. The force platform equipment was computerized. Normal reference values for these measurements are: 39–210 mm2 for the eyes open condition, and 79–638 mm2 for the eyes closed condition [13,14]. The subject stood in a standard Romberg condition on the force platform In all viewing conditions in light, the subject was asked to fixate on a cross in front of the eyes in a distance of 90 cm. 2.3. The main experiment—standard conditions in light Four conditions were tested: a condition with both eyes open (BEO), dominant or non-dominant eye open (DEO and NDEO respectively), and with both eyes closed (BEC). Each condition was done twice, and the order of the conditions was randomized according to the Latin square method. The mean of the results in each condition was used in the statistical analysis. All 28 subjects performed these conditions. They were divided into two groups: the 18 subjects that had normal values in the preliminary tests and the 10 subjects with pathological findings that were excluded from the further analysis. 2.4. Further experiments with vertical prism By this experiment, our aim was to evaluate the relevance of binocular and monocular vision in the control of posture, when the visual input is disturbed by the prism. Eleven of the normal subjects were tested in conditions with a vertical prism placed in front of the dominant eye. This experiment followed the first one after a short pause. At first, the prism (5 D based down Frenzel prism; large enough to cause the disruption of binocular fusion and, hence, diplopia) was E. Isotalo et al. / Auris Nasus Larynx 31 (2004) 11–17 placed in front of the dominant eye, the other eye was covered, and the postural stability was assessed (DEOp). This condition was done twice (the mean of the two measurements was used in the statistical analysis). Then, the subjects performed twice the condition with both eyes open and the prism placed in front of the dominant eye (BEOp) (the mean of the two measurements was used in the statistical analysis). After this, the prism was removed, and the normal binocular viewing condition was assessed (BEO), and also the normal monocular viewing condition with dominant eye open (DEO). An additional experiment was done on a different day with the prism test, in order to see, if the order of the conditions had any effect on the posturographic results. Ten subjects were tested in two different days (in total from 4 to 5 times). The three conditions were: BEOp, BEO, and DEOp. BEO, i.e. normal binocular viewing with the prism removed, was always done between the prism conditions, in order to avoid prism adaptation effects. At different times the test began with either DEOp or BEOp condition. The results from this additional experiment will be reported in the text. 2.5. Statistical analysis In the main experiment, the one-way ANOVA was used to evaluate the effect of non-visual and different visual conditions (BEO, DEO, NDEO, and BEC) on the control of posture at the level of the group of subjects. In the experiment with vertical prism, a two-way ANOVA was used to evaluate: (1) the effect of prism (with and without prism), (2) the effect of ocular condition (binocular versus monocular with dominant eye viewing), (3) the interaction between prism and ocular conditions. The additional prism experiment, in which the order of ocular conditions was counterbalanced, was analyzed with repeated measures ANOVA to evaluate the repeatability of the results. SPSS for Windows 9.0 was used for statistical analysis. 3. Results 3.1. The main experiment, standard light conditions The results of the four conditions (BEO, BEC, DEO and NDEO) for each subject are shown in Table 1. All individual values for all conditions are within the normal ranges [13,14]. There was a large variability of individual performance. Seventeen of the eighteen normal subjects showed better stability in the BEO than in the BEC condition. Our main interest was first in the comparison of BEO condition with the DEO and NDEO conditions. The BEO and NDEO conditions differed significantly/tended to differ out (P < 0.01, <0.05, respectively) from the BEC condition. The DEO and BEC conditions did not differ from each other (P = 0.072). The BEO, DEO and NDEO conditions did not differ statistically significantly from each other. Thus, the 13 only group effect was that the surface area of body-sway was higher in BEC condition compared to that of all visual conditions, which is a classical finding. 3.2. The experiments with prism In the main prism experiment, in DEOp the insertion of the prism in front of the dominant eye increased the body-sway area for all of the subjects. Under BEOp, all the subjects experienced diplopia, in which the horizontal segment of the fixational cross was seen double because the image was displaced upward by the prism. When comparing body-sway area in the BEOp condition with the BEO condition, the body-sway area increased in 7 out of the 11 subjects. This could still be comparable with a monocular effect of the prism. Increased body-sway area in the BEOp condition in respect to both BEO and DEOp conditions was observed only in 2 of the subjects (subjects 8 and 13). Only these subjects might have been to some extent affected by the diplopia caused by the prism rather than by a monocular effect of the prism, even though this effect was not statistically significant at the individual level with repeated measures ANOVA or paired samples t-test. For the rest of the subjects, the differences between individual values of BEO and BEOp were smaller than the differences between BEO and DEOp (Table 2). For the whole group analyzed with two-way ANOVA, the effect of prism factor on the body-sway area was statistically significant (P < 0.005), whereas the effect of ocular factor (both eyes open, dominant eye open) was not (P = 0.652), and neither was the effect of the interaction of these two factors (P = 0.171). In BEOp (=121 ± 62 mm2 ) body-sway area was very similar as in BEO (114 ± 63 mm2 ). The monocular viewing with the prism produced larger value of body-sway area (DEOp = 118 ± 39 mm2 ) than the DEO condition without the prism (75 ± 23 mm2 ), and the difference showed a trend to be statistically significant (P < 0.05 at the individual level, with repeated measure ANOVA and paired samples t-test). In testing the repeatability of the test (with repeated measures ANOVA) in an additional experiment, no significant differences were observed in the body-sway areas of different measurement times in the BEO, DEOp and BEOp conditions. All individual values were within the normal range [13,14]. Thus, postural stability measured during the use of prisms was repeatable and didn’t show any bias in respect to the order of the testing conditions. And, thus the results of the main prism experiment shown in Table 2 can be considered repetitive. 4. Discussion The present study provides evidence that in quiet stance conditions, binocular vision per se in controlling postural 14 E. Isotalo et al. / Auris Nasus Larynx 31 (2004) 11–17 Table 1 Individual data of the 18 normal subjects Postural performance (mean body-sway area in mm2 ) for the standard light conditions (BEO: both eyes open, BEC: both eyes closed, DEO: dominant eye open, and NDEO: non-dominant eye open). Group means and ± standard deviations (S.D.) are shown at the bottom of the table. R: right-eye, L: left-eye. One-way ANOVA between different visual conditions. P-values of significance, NS: non-significant. stability is not a major factor, even for normal subjects with perfect binocular vision and a high degree of stereopsis. This evidence is based on following findings: (1) In standard light conditions, only half of the normal subjects showed better stability under binocular viewing condition than under monocular viewing, and there was no group effect on controlling posture in the three ocular conditions. (2) When a vertical prism was placed in front of one eye, binocu- lar vision was disrupted, and all subjects reported diplopia. Nevertheless, the body-sway area increased only slightly in this condition and for only seven of the eleven subjects. In contrast, under monocular viewing with the prism, the majority of the subjects showed larger body-sway than under BEOp. A vertical disparity created by a prism of 2 D corresponds to about 1◦ and is fusible, whereas it is impossible to fuse the disparity created by a prism of 5 D [15]. The use E. Isotalo et al. / Auris Nasus Larynx 31 (2004) 11–17 15 Table 2 Individual data and group means of the eleven normal subjects tested in the prism conditions Postural performance in BEO: standard binocular viewing without the prism, BEOp: both eyes open, with prism in front of the dominant eye, DEOp: dominant eye open with prism in front of it, DEO: dominant eye open without prism. Postural performance as mean body-sway area in mm2 . Two-way ANOVA with the factor prism (with and without), the factor ocular condition (BEO and DEO), and the interaction between the two factors are shown. P-values of significance, NS: non-significant. of a powerful prism (5 D) aimed to disrupt binocular fusion. The prism experiment provides additional evidence against a major influence of the binocular vision and stereopsis on postural control in quiet stance. (3) Even in dark (in a control study not reported here; confirming the related observations of Fox [8]), the postural stability tended to be better when both eyes were open than when both eyes were covered—i.e. this supports the proposition that binocular vision may not have a major role in postural control during quiet stance. But, however, attention state may differ in these light and dark conditions and may be one cause of this effect [16]. Under dynamic conditions (in perturbed stance), vision per se and binocular vision have most likely a major role in the control of balance in control subjects and in patients [17–20] in contrast to non-perturbed stance in present study. 4.1. Findings of this study in relation to previous studies on quiet stance Fox [8] found that binocular viewing most often attenuates the body-sway more than monocular viewing in differ- ent visual fields. Nevertheless, he also found that in dark the body-sway was lower when both eyes were open than when they were closed in the standard Romberg condition. However, in the tandem Romberg condition the body-sway in binocular and monocular conditions in dark was larger than in the eyes closed condition in dark. He draw the conclusion that the benefit of keeping both eyes open in the control of posture is not due to binocular vision or to stereopsis, but to other mechanisms such as tonicity. We found that better postural stability under binocular viewing than under monocular viewing is not a rule among the normal population in quiet stance. We also confirm the finding of Fox [8] that the benefit of “binocular viewing” is present even in dark, in quiet stance and in standard Romberg position (confirmatory study not reported in the results). The findings of Fox [8] and ours contradict the findings of Paulus et al. [21] who did not find any difference between the body-sway with conditions of both eyes open or both eyes closed in dark. The difference between the studies might be due to the fact that Paulus et al. [21] made modifications to the platform in order to reduce the somatosensory contribution to the 16 E. Isotalo et al. / Auris Nasus Larynx 31 (2004) 11–17 control of posture and to enhance the contribution of the visual and vestibular systems. The results of Guerraz et al. [9] are in line with ours in the fact that, at least, in certain conditions the better postural stability under binocular viewing than under monocular viewing is not a rule among normal subjects. In the study of Guerraz et al. [9], the visual cues consisted of a set of two LEDs mounted in a piece of perspex. The motion parallax reduced the body-sway both in binocular and monocular viewing conditions, and Guerraz et al. [9] postulated that the effect of motion parallax on body-sway was of monocular origin, since it was observed both with monocular and binocular vision. They interpreted that these results support the existence of two modes of visual detection of body-sway, afferent (retinal slippage) and efferent (extra-retinal or eye movement based). Guerraz et al. [9] had a slab of foam rubber under the feet of the subject in all conditions, in order to reduce the proprioceptive contribution to the control of posture and to enhance the contribution of the visual and vestibular systems. This may explain some of the differences of results that were also found between these two studies. Kunkel et al. [10] found, that binocular vision diminished the sway more effectively than any of the monocular vision conditions. Nevertheless, the binocular condition and different monocular conditions were not comparable with each other. Their aim of their study was different from ours, and they did not evaluate the possible differences between binocular and monocular conditions with the different stimuli conditions. These are, however, just speculations that need to be tested. In summary, previous studies addressed the question of benefit of binocular vision in postural stability and presented contradictory results [8–10]. In the present study using the same posturography techniques and the same population, occluding one eye or placing a prism in front of one eye were used to test how these procedures affect postural stability. Findings didn’t show any convincing benefit of binocular vision compared to monocular vision in quiet stance. The results force us to reconcile the existing controversial findings in the literature and to strengthen the conclusion that the effect of binocular viewing on postural stability in quiet stance is subject-dependent. Postural stability is a complex entity controlled by multisensory system, and it is a subject to large individual differences. For instance, there is great individual variation in the relative dependence on either visual information or on the spinal ascending input in controlling posture [25,26]. Similarly, there might be individual variation in the dependence upon binocular or monocular vision. 4.2. Proprioception of extra-ocular muscles and postural stability 4.3. Implications of strabismus for postural control in quiet stance We do not fully understand why some subjects are more stable with both eyes open. It cannot be entirely attributed to the visual input. Perhaps, tonicity of extra-ocular muscles and active force–torques underlying the steady-state primary gaze position, as well as proprioceptive signals from the extra-ocular muscles, play a role and are more important than binocular vision per se. The proprioception of the extra-ocular muscles has been shown to affect the reflexes of balance and the control of posture [22,23], and Eber et al. [23] have proposed the existence of an oculo-oculogyric reflex. According to them, proprioceptive afferents from the extra-ocular muscles are situated in the trigeminal nerve, and project to the trigeminal nucleus. From there, the pathway has connections to the cerebellum, reticular formation and vestibular nuclei. From vestibular nuclei the pathway continues to spinal motor neurons and extra-ocular efferents. Proprioceptive inputs of extra-ocular muscles may also project centrally via the ocular motor nerves [24]. Alternatively, having both eyes open per se in dark could exert some type of contextual influence and mental set capable of acting on the postural stability; postural stability would be better just because the eyes are open, even though, no vision can be used. Earlier posturographic studies of patients with strabismus, as they lack binocular vision and stereopsis, showed no difference in their postural stability under both eyes open and both eyes closed conditions. They were called postural-blind subjects [27]. Also, the strabismic young patients have significantly larger body-sway with eyes open in the light than the control subjects [5,6]. The concept of postural-blindness could be understood as no use of vision at all in the control of posture. That could result from: (1) abnormality in the tonicity of extra-ocular muscles or abnormality in the vestibulo-oculo-postural connections or (2) from the lack of binocular vision. Because even in the subjects with perfect binocular vision there is no major benefit of the stereopsis in quiet stance, we believe that it is the former explanation that is more plausible for the decrease of postural control in strabismic patients rather than the lack of stereopsis. 4.2.1. Postural eye and eye dominance Half of the subjects in our study were found to control postural stability better with one eye viewing in quiet stance (see Table 1). These findings are in line with a prior study of Gentaz [4] that introduced the term “postural eye”. The postural eye is not necessarily the dominant eye (Table 1). 5. Conclusion In quiet stance, among the normal population with perfect binocular vision and stereopsis, only some of the subjects E. Isotalo et al. / Auris Nasus Larynx 31 (2004) 11–17 seem to use binocular viewing to obtain optimal postural stability. With a number of subjects, postural stability with one eye viewing is as good as or even better than with both eyes viewing. Furthermore, the benefit of binocular viewing, present for some subjects may not be due to binocular vision per se or stereopsis. Tonicity of extra-ocular muscles and its influence on the vestibulo-postural connections could be responsible for the lesser body-sway in these subjects in binocular viewing condition than in monocular viewing condition. For example, muscular hypotonicity even when both eyes are open could account for impaired postural stability in strabismic patients [5,6,27], who have normal vision but abnormal alignment. The effect of the prism on postural control seems to be due to its effect on tonicity of muscles rather than its effect on binocular fusion. These findings are limited, however, to the quiet stance conditions studied here. Dynamic postural control is more dependent on binocular vision [17–20]. Acknowledgements E. Isotalo was supported by the Maud Kuistila Foundation (Finland), the Fondation pour la Recherche Medicale (France) and the Otorhinolaryngologic Foundation (Finland). 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