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1 From the Laboratoire de Physiologie de la Perception et de 1'Action. LPPA, CNRS–College de France, Paris, France; 2 Laboratory of Neurobiology of Shanghai Institute of Physiology and Laboratory of Visual Information Processing of Biophysics Institute, Chinese Academy of Sciences, Shanghai 200031, China; 3 Centre Hospitalier National d’Ophthalmologie des Quinze-Vingts (Pr. Nordmann), Paris, France; and 4 Hôpital Robert Debré, Service d’Ophthalmologie, Paris, France.
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Abstract |
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METHODS. Eight subjects were tested (5–15 years old): five with convergent strabismus, three with divergent strabismus. A standard saccade paradigm was used to elicit horizontal saccades to target LEDs (5° to 15°). Saccades from both eyes were recorded simultaneously with the photograph-electric Skalar IRIS device (Delft, The Netherlands). This task was run before and about 3 weeks after strabismus surgery.
RESULTS. Before surgery, the difference in the amplitude of the saccade between the left eye and the right eye was larger (15% of the saccade size) than in normal children of similar age. After strabismus surgery for all subjects the squint angle was reduced, and the amplitude of the disconjugacy of saccades decreased significantly, dropping to normal values (6%). As in normal children, postsaccadic eye drift (both its conjugate and its disconjugate components) was small in amplitude. The difference compared with normal subjects was that disconjugate drift did not restore the disconjugacy of the saccade itself (e.g., in normal subjects drift is convergent when saccade disconjugacy is divergent and vice versa). Rather, disconjugate drift tended to drive the eyes toward static eye misalignment (e.g., the drift was mostly convergent for convergent strabismics and divergent for divergent strabismics). Surgery had no significant effect on either component of the drift.
CONCLUSIONS. The improvement of the binocular coordination of the saccades could be due, at least partially, to central adaptive mechanisms rendered possible by surgical realignment of the eyes. Separate mechanisms control the binocular coordination of saccades and the alignment of the eyes during the postsaccadic fixation period.
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Introduction |
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10°) showed adaptation similar to normal subjects. This contrasts our initial hypothesis and suggests that low-level peripheral vision could be sufficient to drive adaptation of saccade amplitude. To our knowledge studies of binocular motor control in children with strabismus are rather scarce. Inchingolo et al.6 explored the improvement of the postsaccadic eye drift after strabismus surgery, but nothing is known about the quality of the binocular coordination of saccades in such subjects.
In fact, there are very few reference data on the quality of binocular coordination of saccades, even for children without strabismus. The single existing study is that of Fioravanti et al.7
They recorded horizontal saccades from both eyes by using their own infrared limbus-tracking system (Accardo et al.8
). Visually guided horizontal saccades were elicited on an isovergence LED circle, placed at 1 m from the subject. Target jumps were in a range from 0° to 25° with steps of 5°. They examined 12 normal children aged between 5 and 13 years. They showed that binocular coordination of saccades attained the adult characteristics at approximately 10 years: for young children (9 years) saccade disconjugacy was large and usually convergent (1.97°), whereas for older children (
11 years) disconjugacy was small and most frequently divergent as in adults (0.63°). The authors explained these differences by the immaturity of adaptive mechanisms in younger children needed to compensate for ongoing changes and asymmetries of the oculomotor plants.
The goal of the present study was first to examine the natural quality of binocular coordination of saccades in children with moderate to large strabismus. The second objective was to examine possible modifications of the coordination of saccades after strabismus surgery.
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Methods |
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46 
) participated to this 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. Clinical characteristics of each child are shown in Table 1
; subjects are numbered in order of mention in the text of this article. The day before surgery all subjects underwent a complete ophthalmological-orthoptic examination. Corrected visual acuity was 8/10 or better for both eyes for all subjects. Five subjects had convergent strabismus, and, for two of them (subjects 1 and 2), strabismus depended on viewing distance. The three other subjects (subjects 3, 4, and 5) had divergent strabismus that was constant only in subject 5. Strabismus had appeared early (before the age of 2) for four subjects and later for the other four subjects (2, 3, 4, and 6). Only three subjects had binocular visual capability (examined with the TNO test of stereoacuity): subject 6 with late-onset strabismus when corrected with a prism, and subjects 3 and 4 with intermittent divergent strabismus.
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After surgery, at the time indicated in Table 1
(2 weeks to 5 months) another ophthalmological-orthoptic examination was done for all subjects. At this time, the squint angle was reduced considerably (10) for all subjects. Subject 2, with late-onset or acquired strabismus, gained normal binocular vision, and subject 6 improved his stereopsis capability. The two subjects, 3 and 4, who showed stereopsis before surgery maintained the same level afterward.
Eye Movement Recording
The stimulation and the data collection were directed by REX, software developed for real-time experiments and run on a PC. Horizontal eye movements from both eyes were recorded simultaneously with a photoelectric device mounted on spectacles (IRIS; Skalar, Delft, The Netherlands). This system has an optimal resolution of 2'' of arc, a range of 30° for lateral excursion and is linear within 3% for excursions up to 25°. Eye-position signals were digitized with a 12-bit analog-to-digital converter, and each channel was sampled at 500 Hz.
Oculomotor Test
The subject sat in a dark room, viewing binocularly an egocentric arc of LEDs positioned horizontally at eye level 123 cm away. The subject was seated in an adapted chair with a head support. A standard saccade paradigm was used to elicit visually guided saccades: the subject fixated a central small spot of red light (5.6'' of arc); after 800 msec the central spot disappeared and a target appeared for 900 msec at an eccentric randomly chosen position to the left or to the right at 5°, 10°, and 15°. The target was either a normal E or a backward E (0.4 x 0.2°), made by lighting different combination of segments of a seven-segment LED array. The subject was instructed to fixate the target as accurately as possible and to discriminate whether it was a normal E; target presentation was sufficiently long to allow accurate fixation. This task was done twice: the day before strabismus surgery, and 2 weeks to 5 months after the surgery.
Analysis of Data
Calibration and analysis methods are similar to those used in prior adult studies.5
10
Briefly, calibration data were obtained by asking the subjects to fixate monocularly a light-dot presented at various horizontal positions; this was done under both monocular viewing conditions (the other eye was covered). We used monocular viewing for calibration to assure that the subject was fixating the target as precise as possible; recall that, all our subjects had good visual acuity in both eyes and could fixate the target monocularly. This procedure of calibration under monocular viewing is standard used in normal subjects (e.g., Collewijn et al.11
) or in subjects with strabismus but without amblyopia.4
5
6
To confirm further its validity for this study, for three of the subjects (2, 5, and 6), we also calibrated the data with factors extracted from a binocular viewing condition. The results produced with the two methods of calibration were almost identical. A linear function was used to fit the calibration data. From the fixation periods between saccades, i.e., at the end of each trial, we measured the eye misalignment, i.e., the degree of squint before and after surgery: the left–right eye position difference; positive values indicate convergent strabismus, negative values divergent strabismus.
Saccade onset was determined at the point where eye velocity reached 5% of the peak velocity; saccade offset was taken as the time when eye velocity dropped below 10°/sec.
For each saccade we examined the binocular coordination by measuring the amplitude of the disconjugacy, i.e., the left eye–right eye difference; we also measured the gain (saccade amplitude/target excursion, in degrees). The amplitude of the postsaccadic eye drift was measured over the period after the offset of the primary saccade until the onset of a corrective saccade. Most of the saccades were followed by a corrective saccade with latency between 180 and 350 msec. Thus, our measure of postsaccadic drift covered on average a period of 241 msec. Postsaccadic eye drift could continue after the corrective saccade or change its direction (see examples, Fig. 2 ). In this respect, our study of the drift is not exhaustive, but it is meant to describe the quality of binocular fixational stability in the first period after the primary saccade, which is important to process visual information immediately after the saccade. The amplitude of the drift was measured for each eye; from these measures we estimated the conjugate or cyclopean component of the drift: [(amplitude of the drift of the left eye + amplitude of the drift of the right eye)/2], and the disconjugate component, i.e., the difference in the amplitude of the drift between the left and the right eye. The disconjugacy of the saccade and the two drift components (conjugate and disconjugate) were always expressed as a ratio of the amplitude of the saccade. This was because inspection of our data indicated, at least for some subjects, a tendency for the disconjugacy to increase for larger saccade amplitudes. Note also that the same range of target excursions was used for the before and after surgery oculomotor test, and the mean amplitude of saccades obtained was similar before and after surgery (12.6 ± 2.5° and 13.1 ± 2.7°, respectively). Two types of analysis were done: one on the absolute value of the different measures, and a second on algebraic data, taking into account the sign of the disconjugacy. The sign of the disconjugate component of the postsaccadic drift was as follows: positive differences (left–right eye) indicate convergent disconjugacy and negative values divergent disconjugacy, regardless of the direction of the saccade. To evaluate the speed of saccades we measured the ratio of peak velocity over the amplitude of the saccade for each individual eye, before and after surgery.
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Results |
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) than the value of strabismus measured clinically, and the postsaccadic drift was small. The left, dominant eye was the eye fixating the target. As shown by the disconjugacy trace, the execution of the saccades was associated with a disconjugacy or sudden change of the squint that was very variable, divergent, or convergent. Two weeks after surgery (Fig. 2B)
the static deviation was considerably reduced to approximately 1° (approximately 2), but convergent postsaccadic drift was still seen after some of the saccades shown. Note that the disconjugacy of the saccades was of smaller size and almost always divergent (downward inflection of the trace).
Quantitative Data.
In Fig. 3A
is shown the average amplitude of the disconjugacy of saccades expressed as ratio of the saccade amplitude (absolute values). Data are shown before and after surgery for each subject. Before surgery, the ratio was higher than 0.1 for all subjects. The highest values were observed for the two younger subjects (1 and 2), and for the two older subjects who had large strabismus (subject 6: 46 ET, and subject 5: 30 X). The mean ratio was 0.16 ± 0.05; this value is higher than that reported by Fioravanti et al.7
in children without strabismus of corresponding age (approximately 0.10 for saccades of similar amplitude).
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In normal adults, the disconjugacy of saccades increases under monocular viewing, relative to binocular viewing.10 We tested this aspect in five of the subjects (1, 2, 3, 5, and 6), who performed the saccade task under binocular viewing and under both monocular viewing conditions (see Table 2 ). Contrary to normal subjects, in our subjects, the disconjugacy of saccades did not vary significantly with the viewing condition either before (F2,8 = 0.18, P = 0.83) or after surgery (F2,8 = 3.22, P = 0.09).
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Postsaccadic Eye Drift
Figures 3B
and 3C
, show the conjugate and disconjugate components, respectively, of the postsaccadic eye drift expressed as a ratio of the amplitude of the saccades. Data are shown for each subject before and after surgery.
Conjugate Component.
Before surgery, the drift was small in all subjects. The group mean ratio was 0.04 ± 0.03, and individual ratios ranged between 0.01 and 0.04, except for subject 7 (0.12 ± 0.09). Surgery had no significant effect on the conjugate drift (F1,7 = 0.02, P = 0.88; Fig. 3B
). At the individual level (see asterisks in Fig. 3B
), there was a significant decrease of the amplitude of the drift relative to the before values for subjects 6, 7, and 8 and a significant increase for subject 1. Note that subjects 1, 7, and 8 had all early-onset strabismus, yet drift decreased in two of them (subjects 5 and 7) and increased in subject 1, indicating no consistent pattern. Thus, overall, the conjugate drift was small in amplitude before as well as after surgery. Our observations are compatible with the study in normal children,7
showing that conjugate drift, at least for small saccades (10°), is small.
Disconjugate Component.
The amplitude of the disconjugate postsaccadic drift was also small for all subjects (Fig. 3C)
; the group mean ratio was 0.06 ± 0.02 (range of individual ratios, 0.02–0.09). For five subjects, the sign of the drift (not shown in the figure) was on average in the direction of the static offset of the eyes: drift was on average convergent for three of the five subjects with convergent strabismus (1, 2, and 8) and divergent for two of the three subjects with divergent strabismus (subjects 3 and 5). This is in agreement with the findings of Inchingolo et al.6
in children with strabismus. Thus, in normal subjects, drift restores or reduces the disconjugacy created by the saccade, whereas in children with strabismus drift drives the eyes to the default position of the misalignment.
Strabismus surgery had no significant effect on the amplitude of the disconjugate component of the drift (absolute values, F1,7 = 2.76, P = 0.14); at the individual level there was no significant surgery effect for any of the subjects. There was no significant effect of surgery on the sign of the drift disconjugacy either (ANOVA was applied on the algebraic values of drift disconjugacy, F1,7 = 1.64, P = 0.24).
Speed of Saccades
Table 3
shows individual mean peak velocity normalized by the amplitude of saccades for the dominant and for the nondominant eye before and after surgery. Before surgery, the highestvelocities were observed for the two younger subjects (1 and 3); this is compatible with observations in normal children for increased velocity of saccades in younger children relative to that of older children.7
After surgery, saccades of the dominant eye became significantly slower for two subjects (6 and 7, Student’s t-test comparing before–after surgery mean of normalized peak velocity, significant at P < 0.05); for the nondominant eye, the after surgery decrease of velocity was significant for three subjects (5, 6, and 7). There was no significant effect for the remaining five subjects. For the ensemble of the subjects, ANOVA showed no effect of the surgery in the velocity of saccades (F1,7 = 1.88, P = 0.21 for the dominant eye and F1,7 = 3.40, P = 0.11 for the nondominant eye).
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Discussion |
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Effects of Surgery
Strabismus surgery was, at least at the time of our testing, successful because the static eye deviation was considerably reduced for all subjects, and one became orthotropic. Binocular vision recovered only for two of the four children with late-onset strabismus (subjects 2 and 6). The second effect of the surgery was that the disconjugacy of the saccade was significantly reduced relative to the before-surgery values. The reduction occurred systematically regardless of the type of strabismus. In addition, the sign of the disconjugacy (convergent or divergent) became less variable than that observed before surgery.
The improvement in the conjugacy of saccades could be the direct consequence of the surgical realignment of the eyes, but most likely, it was mediated by central adaptive mechanisms, e.g., more efficient tuning of motor commands when the two eyes are aligned. In particular, the decrease of the variability of the sign of the disconjugacy argues in favor of central adaptation. Indeed, in normal adults, the existing disconjugacy of the saccades is almost systematically divergent. It has been argued that this stereotyped aspect is the result of central adaptation to properties of oculomotor plants and/or of premotor circuits innervating the lateral rectus and the medial rectus muscles (see Fioravanti et al.7 ).
If one admits the hypothesis of central adaptation, one should address the question to what extent the improvement of saccade conjugacy by surgery reflects a modification of the preferred retinal loci for positioning the eyes or a higher level binocular remapping of retinal space, leading to better motor conjugacy. Indeed, there is early evidence for a covariation of strabismus angle and retinal correspondence.2 13 14 For subjects like subjects 2 and 6, who improved binocular vision, a binocular remapping presumably occurred and could be at the origin of the improvement of saccade conjugacy. A similar mechanism could take place even for the subjects whose strabismus was reduced but who did not develop normal measurable stereopsis (subjects 1, 5, 7, and 8). Finally, the finding that the disconjugacy of saccades did not change significantly under different viewing conditions suggests a relative constancy in the preferred retinal loci regardless of the viewing conditions. Nevertheless, our eye movement recordings do not allow to substantiate this important issue of change in preferred retinal loci before and after surgery.
Whatever the mechanism is, this study shows for the first time, dynamic harmonization of binocular coordination of saccades after strabismus surgery. The stability of this effect over time remains to be studied.
Postsaccadic Eye Drift in Strabismus
Before surgery, both the conjugate and the disconjugate component of the postsaccadic drift were small, less than the disconjugacy of the saccade itself. The surgery had no effect on the postsaccadic drift for either component.
An important aspect emerging from the ensemble of our observations is that the binocular coordination of the saccade and the binocular coordination of the drift are controlled by separate mechanisms. This is compatible with earlier monkey studies on adaptive control of saccade amplitude versus postsaccadic drift15 and in humans16 17 ; saccade amplitude adaptive control requires readjustment of the saccade, i.e., pulse and step signals together, whereas the postsaccadic drift involves readjustment of the ratio of these components. The above-cited studies deal with conjugate mechanisms; disconjugate mechanisms controlling the postsaccadic drift could be more complex. As pointed out by Fioravanti et al.7 the adaptive mechanism controlling the drift differently for the two eyes could be more complex and would develop later in normal children than the mechanism that control the amplitude of the saccades. In this context, our observations of the invariance of the drift in children with strabismus could be seen either as due to the immaturity of the corresponding adaptive ability or to its longer time course. Nevertheless, one should take into account that the major abnormality was in the amplitude of the saccades and this disconjugacy was decreased after surgery, thereby reducing the disparity present at the end of the saccade and thus the need for postsaccadic corrective mechanisms.
Stimulus Driving Postsaccadic Drift and Saccade Amplitude Adaptation
Our findings for the drift contradict the observations of Inchingolo et al.,6
who found, for all subjects, significant decrease of the drift after surgery. Even though several methodological differences between the two studies exist (e.g., age of subjects, type of surgery, and evaluation of the drift over longer periods including after secondary saccades), the different results could be due to the fact that in the study of Inchingolo et al.,6
binocular fusion was regained after surgery by all subjects. In other words, fusion could be necessary for activating the adaptive mechanism needed to reduce disconjugate postsaccadic drift. Disruption of fusion and postsaccadic retinal slip are the two signals that could drive disconjugate drift adaptation. Indeed, Kapoula et al.17
showed that visually induced adaptation of horizontal postsaccadic drift (by drifting the images at the end of the saccade) is not possible when the images viewed by the two eyes cannot be fused. This is in contrast with a subsequent study in monkeys18
showing that disconjugate adaptation of vertical postsaccadic drift is possible even without fusion. There might be differences, however, in the respective role of fusion and retinal slip for the horizontal and vertical adaptive system. Thus, on the basis of the data available in human studies for horizontal postsaccadic drift, we suggest that fusion might be necessary for postsaccadic drift adaptation, whereas it could be less critical for saccade amplitude adaptation. Most likely, low-level peripheral binocular or bi-ocular vision could be sufficient to drive such type of adaptation.5
This is reminiscent of the capacity to trigger disparity vergence eye movements even when using different images for the two eyes (a circle and a cross; see Westeimer and Mitchell19
).
Speed of Saccades
The speed of saccades for the majority of the subjects (n = 5) did not change after surgery. This finding is in agreement with the few reports available in the literature exploring in children the change of velocity of saccades after small recession of one eye muscle,20
21
similar to those applied in our study. At the individual level, however, the saccades of three subjects (5, 6, and 7) became significantly slower. A similar phenomenon of slowing down of saccades has been reported by Lewis et al.22
in adults with congenital or with acquired oculomotor paresis. Two months after surgery, static eye alignment improved as well as binocular coordination of the saccades, and saccades were found to be slower relative to the presurgery values. The authors attributed these effects to central adaptation. Our observations are also compatible with studies dealing with visually induced oculomotor adaptation of the gain of the saccades in monkeys,23
or, more recently, in humans:24
adapted saccades were reported to be slower. Thus, the decrease of saccade velocity reported in this study for three subjects could also be mediated by central adaptive mechanisms compensating for the changes in the oculomotor plants.
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Acknowledgements |
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Footnotes |
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Submitted for publication May 21, 2001; revised November 2, 2001; accepted November 30, 2001.
Commercial relationships policy: N.
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. 
1734 solely to indicate this fact.
Corresponding author: Maria Pia Bucci, Laboratoire de Physiologie de la Perception et de 1'Action, UMR 9950, CNRS-College de France 11, place Marcelin Berthelot, 75005 Paris, France; maria-pia.bucci{at}college-de-france.fr
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