Binocular coordination of saccades is essential for clear vision. It allows the object of interest to fall on the fovea of each eye, which is a prerequisite for fused single binocular vision. Kapoula, Robinson, and Hain (1986) reported for the first time that the ending of horizontal saccades is asymmetric for the two eyes: the adducting (nasally directed) eye drifts nasally in the direction of the antecedent saccade, while the abducting eye has a backward small zero-latency saccade, the so-called dynamic overshoot, that causes the eyes to converge at the end of the saccade. If the eyes converge at the end of saccades, they must diverge during the saccades. Collewijn, Erkelens, and Steinman (1988) confirmed this prediction with high-quality binocular recordings. They reported substantial divergence of the eyes at the beginning of the saccade; and, at the offset of the saccade, there is still a residual divergent disconjugacy. The authors argued that the binocular disparity created by the disconjugacy can not compromise binocular vision given its small amplitude (< 1^o). However, subsequently, Collewijn, Erkelens, and Steinman (1997) reported that in adults, saccade disconjugacy is more severe at close viewing distance; they attributed this to geometrical considerations (a small lateral displacement of the eyes corresponds to a large angle at close distance). It is important to recall that this aspect (i.e., the dependency of saccade disconjugacy upon viewing distance) is of particular significance for many situations of visual ergonomy (e.g., screen working and reading, because such activities take place at close distance).

Binocular coordination of saccades is particularly important for children, especially when they begin to read. Indeed, Fioravanti, Inchingolo, Pensiero, and Spanio (1995) reported that binocular coordination of saccades is poor in young children. Although in adults saccadic disconjugacy is stereotyped, most of the time it is divergent. In young children, disconjugacy is of variable sign (i.e., sometimes convergent and other times divergent). Furthermore, the amplitude of the disconjugacy is substantially larger than that of adults. These authors also described increased disconjugate post-saccadic drift in children. The binocular coordination during and after the saccades achieves adult levels only at about 10-12 years old.

The distance at which subjects made saccades in the study of Fioravanti et al. was 100 cm. To our knowledge, the quality of binocular coordination of saccades in near vision for children has not been examined; recall that reading distance is about 30-40 cm. Studies dealing with learning difficulties in reading and dyslexia suggest that poor coordination of the eyes during and after the saccades could be involved in the etiology of reading problems (Stein, Riddell, & Fowler, 1989). The first objective of this study was to provide reference data in young children on the quality of binocular coordination of saccades at close distance in a simple oculomotor task. Does proximity influence the binocular coordination the same way in adults and in children? To respond to these questions, this work compares binocular coordination of saccades in children and in adults at two distances (20 and 150 cm).

Fourteen children and 10 adults participated in this experiment. The children’s ages ranged from 4.5–12 years: 6 children 4.5–6 years old; 4 children 7–8 years old; and, 4 children 10–12 years old. The adult’s ages ranged from 22–44 years (28.1 ± 6.2 years). All children had normal vision, and none wore spectacles. Adult subjects were all emmetropic (no refractive errors). No subjects showed visual, neurological, or psychiatric disorders or received medication. All subjects had normal motility and normal ocular alignment. Binocular vision was assessed with the Netherlands Organization of Applied Scientific Research test of stereoacuity (TNO); all individual scores were normal, 60" of arc or better. The investigation adhered to the tenets of the Declaration of Helsinki and was approved by the institutional human experimentation committee. Informed consent was obtained from adults and children’s parents.

The experimental task was explained to the subjects and to children’s parents before the experiments. Subjects were requested to move their eyes to the light-emitting diodes (LEDs) as soon as possible and as accurately as possible after the target appearance but not before. The subject’s head was stabilized with a chin rest.

LEDs data collection was directed by REX software that was developed for real-time experiments and runs on a PC. Horizontal movements from both eyes were recorded simultaneously with a photoelectric device (oculometer; Bach, Bouis, & Fischer, 1983).The eye is homogeneously illuminated by infrared light. The infrared picture of the eye is projected on a special detector. From the outputs of this detector, eye position is electronically computed both in the horizontal and in the vertical directions. This system has a resolution of 1 to 5 min of arc and linear range of ±20 deg. There is no obstruction of the visual field with this recording system (Bach et al., 1983). The accuracy of this system is between 5 and 10 min of arc when the subject’s head is restricted well. Eye-position signals were digitized with a 12-bit analogue-to-digital converter, and each channel was sampled at 500 Hz.

The visual display consisted of LEDs placed at two isovergence circles: one at 20 cm from the subject, and the other at 150 cm. On the close circle, three LEDs were used; one was at the center and others were at ±20°. On the far circle, five LEDs were placed: one at the center, two at ±10°, and two at ±20° (see Figure 1A). The disconjugacy for saccades in either distance decreases significantly with the children’s age and reaches adult values at the age of 10–12 years. Complementary results about the sign of children’s saccade disconjugacy are shown in Table 1. For adults, the disconjugacy is predominantly divergent, 80% and 84% for saccades at close and at far, whereas for children this percentage is smaller and increases gradually. These observations are in agreement with the study of Fioravanti, Inchingolo, Pensiero, and Spanio (1995). For post-saccadic drifts, the rates of occurrence of divergent disconjugacy are similar for children and for adults, and there is no consistent trend over children’s age.

In summary, the data examined across children’s ages show substantial development of the two parameters describing the binocular coordination, that is, the disconjugacy of the saccades and the disconjugacy of post-saccadic drift. The most dramatic improvement occurs at 7–8 years old, approaching adult values at 10–12 years old.

This study demonstrated that the binocular coordination of the eyes during the saccade and after the saccade is poor in children, especially for the youngest children (4.5–6 years old). The results are in agreement with prior studies (Collewijn et al., 1988; Fioravanti et al., 1995). The new finding here is that the saccade disconjugacy in children is dramatically deteriorated at close distance, more than it was known for adults (Collewijn et al., 1988).

The disconjugacy of saccades for children, particularly at close distance, could be considered a violation of Hering’s law, according to which the yoking pair of muscles of the two eyes receives equal innervation so that both eyes move together like a single organ. During the past decade, there has been extensive evidence showing some disconjugacy of saccades even for adults (Collewijn et al., 1988; Kapoula, Eggert, & Garraud, 1997).For some authors, such disconjugacy provides evidence against the existence of this law; such a view is supported by physiological studies that indicate that premotor neurons in the paramedian pontine reticular formation (PPRF) may encode saccade signals monocularly (Zhou & King 1998). Nevertheless, another view is that Hering’s law is basically true but imperfect, and can only grossly assure the coordination of the two eyes. Learning and adaptation are needed for the fine tuning of motor commands for each eye to enable normal quality of binocular coordination in adults. Learning is believed to be activated by the detection of errors by the visual system; binocular disparity at the end of saccades is probably the major error (Kapoula, Eggert, & Bucci, 1995; Kapoula, Bucci, Lavugne-Tomps, & Zamfirescu, 1998). On the other hand, disruption of binocular vision disables such learning-adaptive mechanisms. Indeed, both children and adults with strabismus and without binocular vision have decreased binocular coordination relative to normal subjects (Kapoula et al., 1997; Bucci, Kapoula, Yang, Roussat, & Brémond-Gignac, 2002). Consistently decreased adaptive capabilities to disparity images were reported in subjects with large strabismus (Bucci, Kapoula, Eggert, & Garraud, 1997).

Why is binocular coordination poorer at close distance? As mentioned, Collewijn et al. (1997) attributed the increase of saccade disconjugacy at close distance to geometrical reasons. Our study indicates that the influence of distance on saccade disconjugacy is more pronounced for children than for adults and is not compatible with the geometrical consideration hypothesis. Most likely, at close distance there is a central interaction between saccades and the control of vergence. Children have to learn to tailor the saccade commands with the eyes converged at close distance to maintain the convergence angle during and after the saccades.

An alternative interpretation of the disconjugacy in younger children and its decrease with age should be discussed. Indeed, one could argue that disconjugacy results from naturally existing asymmetries of the oculomotor plants (e.g., differences in the transition function of the internal and external recti). Any muscular differences could be particularly reflected in the dynamics of the saccades, such as the peak velocity. We examined the difference for peak velocity of saccades between the two eyes in children and in adults. The data show that the disconjugacy of peak velocity is 53 ± 22°/s and 55 ± 25°/s at far and at close distance in children. Our observations are in line with those of Fioravanti et al. (1995). These values for adults are 44 ± 17°/s and 52 ± 22°/s at the two viewing distances. Although the values for young children tend to be higher than those for adults, the difference is not statistically significant for either viewing distance (t test: t₂₂ = 1.72, p = .10, and t₂₂ =0.26, p = .79, for far and close distance, respectively). Most important, there is not significant difference between far and close for adults (t₉=1.71, p = .12) or for children (t₁₃ =0.71, p = .49). These data clearly contradict those on the disconjugacy of the amplitude of the saccades and indicate that the disconjugacy of amplitude and of the peak velocity of saccades do not result from the same factor. Particularly, the relative invariance of disconjugacy of peak velocity with viewing distance contrasted with the increase in disconjugacy of the amplitude indicates that saccade amplitude disconjugacy cannot be accounted by muscular differences alone. Finally, the muscular asymmetric hypothesis considered above is incompatible with physiological knowledge (e.g., studies of saccades pointing out that the premotor and motor circuitry are already mature by 4 years old (Cohen & Henn, 1972; Fukushima, Hatta, & Fukushima, 2000). Asymmetric peak velocities of left and right eyes (adducted > abducted saccades) have been reported in some early studies using electro-oculography (Boghen, Troost, Daroff, Dell'Osso, & Birkett, 1974; Bird & Leech, 1976), but other studies using the infrared reflection technique provided opposite results (Fricker & Sanders, 1975; Hallett & Adams, 1980). Thus, there is no clear evidence for systematic asymmetry of peak velocity of abduction and adduction relative to the muscular properties. One should notice here that the work on other types of eye movements (e.g., horizontal pursuit) shows nasal-temporal asymmetry in young infants, particularly for the infants with congenital strabismus esotropia (Tyschen & Lisberger, 1986). However, even in that case, the asymmetry is believed to be due to cortical immaturity of visual motion-processing systems, the temporal motion relying on later cortical development of corresponding visual areas. In conclusion, the distance-dependant disconjugacy of the amplitude of saccades is most likely due to immature cortical or subcortical control of saccade signals when the eyes are converged than to muscular difference between the two eyes.

This work shows that the binocular coordination of saccades is not built-in but is a process developing through visual experience and learning. Most important, learning to improve saccade coordination also includes adjustment relative to distance (i.e., control of both vergence and saccade signals). A teleological argument would be that disconjugacy of the saccades in young children, particularly at close distance, is deliberate: it would help to stimulate and implement the adaptive learning mechanisms, which are needed throughout life to maintain good binocular coordination. Learning mechanisms are needed even in the absence of severe disorders to adapt to new spectacles, or to maintain good performance. Thus, the disconjugacy showed by the youngest children provides an image of the range of adaptive abilities that needed to be developed.

Increased disconjugacy at near distance might be interfering with vision, and word reading. Stein, Richardson, and Fowler (2000) reported that children with reading difficulties (dyslexics) tend to have inferior binocular coordination and poorer vergence control than normal readers. They also pointed that dyslexics could improve their reading ability by improving their binocular stability with orthoptic exercising. Our findings support such vision because even for the normal younger children, the disconjugacy of the saccades at near is substantial (about 2^o, see Figure 2B) and could interfere with reading. Namely, it could slow down word recognition until the eyes are appropriately aligned in the word.

Importantly, drift of the eyes and disconjugacy of the drift are also significant in children and for either viewing distance (see Figure 2C). These observations are in agreement with the study of Fioravanti et al. (1995). The drift amplitudes (conjugate and disconjugate) found in children over the period of approximately 160 ms following the end of the saccade and before the onset of corrective saccade (see “Methods”) was ≥ 0.5^o. Drift velocity could thus be ≥ 3^o/s. It is known that visual acuity degrades when image velocity exceeds 2^o/s (Westheimer & McKee, 1975). Thus, poor stability and alignment of the eyes during fixation are other factors that could interfere with clear vision. Once again, the slowness of beginner readers could be partially due to such physiological imperfections of the binocular coordination of eyes during and after every saccade. Further studies of the binocular coordination of the saccades during reading tasks are needed, however, to consolidate this point.

The authors thank Dr. M. P. Bucci for conducting some of the recordings of eye movements and for comments on the manuscript. The work was conducted at the children’s hospital Robert Debré in Paris, Departments of Otorhinolaryngology (Dr. S. Wiener-Vacher) and Ophthalmology (Dr. D. Bremond-Gignac). Q. Y. was supported by the French Ministère de la Recherche et de la Technologie and Centre National de la Recherche Scientifique–K. C. Wong. The research was supported by the Institut National de la Santé et de la Recherche Médicale (grant no. 4M105E) and the MRT Dysfunctioment cognitif (coordinated by F. Vitu). Commercial relationships: none.