role of attention and eye preference in the binocular coordination of saccades in strabismus
TRANSCRIPT
115Attention and saccade coordination in strabismus
Correspondence and reprintrequests to:Dr. Zoï KapoulaLaboratoire de Physiologie de laPerception et de l’ActionUMR 9950CNRS-Collège de France11 place Marcelin BerthelotF-75005 ParisFranceTel: +33-1-44-27-16-35Fax: +33-1-44-27-13-82e-mail: [email protected]
Acknowledgements:Pr. M. Bernotas was supported byFrench Medical Research Foundation.We thank the subject of this study forher cooperation and Dr. E. Isotalo forimproving the form of the manuscript.
Original paper
Neuro-ophthalmology 0165-8107/99/US$ 15.00
Neuro-ophthalmology – 1999, Vol. 22,No. 2, pp. 115-126© Æolus Press 1999
Accepted 18 June 1999
Role of attention and eye preference in thebinocular coordination of saccades in
strabismus
M.P. Bucci1
Z. Kapoula1
M. Bernotas2
F. Zamfirescu3
1Laboratoire de Physiologie de la Perception et de l’Action,UMR 9950, CNRS-Collège de France and 3Hôpital Saint-
Antoine, Service d’Ophtalmologie, Paris, France2Siauliai University, Siauliai, Lithuania
Abstract This study examines squint change and the binocular co-ordination of horizontal and vertical saccades in an adult subject withincomitant strabismus (20 or 40 prism diopters) strongly depending onthe eye used for fixating. The patient had no binocular vision and wasdiagnosed ‘horror fusionis’ since her childhood. We found the angle ofhorizontal squint to be smaller when the patient was fixating with thepreferred eye than with the nonpreferred eye. The squint was smallerwhen both eyes viewed and one eye fixated attentionally than when thenonfixating eye was closed. This suggests the importance of binocularvisual stimulation. We found no significant changes in the amplitude ofthe disconjugacy of the saccades. However, when the preferred, lefteye fixated attentionally (under binocular viewing) or monocularly, thepattern of the disconjugacy changed: the majority of the saccades showeddivergent disconjugacy. This pattern is qualitatively similar to that seenin normal subjects. In this patient, divergent disconjugacy helped todecrease the convergent squint at the end of the saccades. Interestingly,vertical squint was small and did not depend on viewing conditions.The binocular coordination of vertical saccades was almost normal, atleast in the binocular viewing condition. We conclude that the visualinput from both eyes allows a rudimentary binocular cooperation thathelps to keep the squint small and renders disconjugacy of horizontalsaccades strategically divergent to reduce temporally the squint.
Key words Saccades-disconjugacy; attention-eye preference; stra-bismus; binocular vision; disconjugate adaptation
Introduction Binocular motor coordination is necessary to achievebinocular bifoveal vision. Kapoula et al.1 showed that the binocularcoordination of horizontal saccades is significantly impaired in subjects
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with large convergent strabismus without binocular vision. The coordi-nation of the eyes during and after the saccade is further impaired whenthe patients are forced to fixate with their habitually nonpreferred eye.In contrast, De Faber et al.,2 who studied subjects with divergent stra-bismus and important unilateral amblyopia, did not find a significantdifference in the conjugacy of saccades depending on which eye wasviewing the target. Maxwell et al.3 examined the conjugacy of saccadesin 11 subjects, most of them with convergent strabismus and with deepunilateral amblyopia. They found saccadic yoking to be worst when theamblyopic eye was covered compared to when both eyes were viewing.The authors suggested that the low visual information received fromthe amblyopic eye can, however, be important for the binocular controlof the saccadic system. Such observations suggest that the binocularcoordination of saccades in patients with disrupted binocularity, al-though primarily driven by monocular visual input, can still benefitfrom binocular visual stimulation. The issue is of major theoreticalimportance related to the question of the importance of binocular ver-sus monocular visual input controlling the binocular motor control innormal subjects and in patients. Eye preference may be important forbinocular motor control even in subjects with normal binocular vision.Kapoula et al.4 showed that the coordination of the eyes during a sac-cade and during the early period after a saccade is dependent uponwhich eye is fixating the target during the recording period.
To gain more insight on the importance of monocular versus binoc-ular visual inputs on binocular motor coordination, we examined thedegree of yoking of horizontal and vertical saccades in an adult subjectwith convergent strabismus and ‘horror fusionis’ since her childhood.The term ‘horror fusionis’ was first used by Bielschowsky5 for subjectswho reject any sort of bifoveal input and show complete deficiency ofsensory binocular fusion; it could be due to a defective development ofsensory connections in the visual cortex.6 In our patient, visual acuitywas good in both eyes, but binocular vision was completely absent. Thepatient could alternate the fixating eye rapidly at will. Her squintmeasured by orthoptic clinical tests increased by as much as 20 prismdiopters, when she was choosing the right, nonpreferred eye to fixate.To examine attentional influences, we estimated the squint change withobjective eye movement recordings in several binocular viewing con-ditions during which the subject was asked to choose one or the othereye for fixation. The squint under monocular viewing was also mea-sured. We found the squint to be significantly smaller when both eyeswere viewing than when one eye was viewing. In agreement with theorthoptic tests, we found the squint to be less when the preferred eyefixated attentionally or monocularly than when the nonpreferred eyefixated. Most important, the changes in the squint caused instantaneouschanges in the quality of the binocular coordination of saccades. Wealso report an experiment showing that the patient was not able tomodify the natural pattern of saccade coordination when exposed tovisually imposed aniseikonia, a task rapidly achieved by normal sub-jects.
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117Attention and saccade coordination in strabismus
Materials and methods
clinical characteristics of the patient The patient was afemale, 31 years old. Convergent strabismus appeared at the age of 2.5years. At the age of 3.5 years, she underwent eye surgery. At the timeof our examination, she had an esotropia of 20-40 prism diopters forboth distant and near fixation and a hypodeviation of the right eye of12 prism diopters (measured by the cover-uncover test, prism, the syn-opthophore, and the Weiss test – a test similar to the Lancaster test).The amount of horizontal deviation depended on which eye was fixat-ing: 20 prism diopters when the left eye was fixating and 40 prismdiopters when the right eye was fixating. She had no V or A pattern;the hypotropia of the right eye was constant (12 prism diopters) at allgaze positions and did not depend on the fixating eye. Daily, the pa-tient generally used her left eye to fixate except when tired.
The after-image test of Bielschowsky showed the presence of normalretinal correspondence. All tests of binocular vision (TNO random dottest for stereoacuity, Titmus, Worth 4-dot test and the synoptophore)were negative and showed no capacity of binocular vision. The patientcould not tolerate spectacle correction and was diagnosed for ‘horrorfusionis’ in her childhood.
In conclusion, the patient had no binocular vision, and the variationof her squint according to the fixating eye was unusually large.
oculomotor testing Visual stimulation, eye movement record-ing, and data analysis were similar to those described elsewhere byKapoula et al.7 Briefly, the patient sat in a dark room 1 m in front ofa flat, translucent screen. The head was stabilized by using a bite barand a forehead support. A standard visually guided saccade paradigmwas used. The target moved in some conditions horizontally and inother conditions vertically from 0 deg to a randomly chosen eccentricposition (±5, ±10, ±15, ±20 deg) to the left or to the right, upward ordownward along the midline. The target used was a pair of noniuslines, i.e. two parallel vertical lines separated by a distance of 5 minarc. Nonius lines were used to encourage accurate fixation: the subjectwas instructed to fixate as accurately as possible between these twolines. Horizontal saccades were recorded under five different condi-tions. In the first condition, the patient fixated binocularly and did notreceive any instruction (natural binocular viewing, BEV). In the subse-quent two conditions, the viewing remained binocular, but in eachcondition the patient was asked to attentionally fixate the targets eitherwith her right nonpreferred eye or with her left preferred eye (BEVREFand BEVLEF conditions). Finally, in two other conditions, one eye wascovered (left eye viewing = LEV, right eye viewing = REV). Verticalsaccades were recorded in the natural binocular viewing (BEV) and inthe two monocular viewing conditions (REV, LEV). Each conditionlasted about 2 min, and one succeeded another at the rate of 2-3 min.Therefore, the reported changes in saccade coordination and squintreported were almost instantaneous.
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eye movement recording Horizontal and vertical saccades of thetwo eyes were recorded simultaneously with the search coil-magneticfield method.8,9 The eye position signals were filtered with a bandwidthof 0-200 Hz, digitized with a 12-bit analog-to-digital converter sam-pling each channel 500 times per second. Overall effective systemsensitivity was 0.05 deg. At the beginning of the experimental session,each eye was calibrated individually by fixating the target monocularly.
data analysis Measured eye-position data were corrected for theintrinsic sine nonlinearity of the coil system and for the tangent screeneffect; the viewing distance was taken into account for calibration.Saccade beginning and end was determined by algorithms based onvelocity and acceleration criteria; saccade onset was determined at thepoint when eye velocity reached 5% of the peak velocity; for the sac-cade end at the point when eye velocity dropped below 10 deg/sec. Theamplitude of postsaccadic drift was averaged over the period of 600msec after the end of the saccade. The alignment of the eyes (the angleof squint) was measured at the beginning of the saccade, just afterthe end of the rapid pulse component of the saccade and at the end ofeach postsaccadic fixation period (about 600 msec after the saccade).The disconjugacy (LE-RE difference in degrees) of the amplitude ofthe saccade and of the postsaccadic drift was measured for each saccade.We call intrasaccadic disconjugacy the difference in the amplitude ofsaccades. Statistical analysis was performed by using the Student’st-test.
Results
coordination of horizontal
Qualitative observations Figure 1 shows binocular recordings of asequence of saccades made by the patient under the three differentbinocular viewing conditions tested. It shows remarkable instantaneouschanges not only in the squint angle, but also in the coordination ofsaccades depending on which of the two eyes was attentionally used forfixation. The deviation of the eyes was always convergent as shown bythe trace of the disconjugacy that was always positive. Under naturalBEV, the squint averaged over the 10 seconds was 14.1±1.3 deg (cor-responding to 24 prism diopters). Saccades were disconjugate (see peaksof disconjugacy during the saccades) and followed by a significantdrift. When the patient fixated attentionally with the right, nonpreferredeye (BEVREF), the squint increased instantaneously (the mean valueover the 10 seconds was 19.9±2.3 deg, i.e. 34 prism diopters). In thenext two minutes, when the subject fixated attentionally with the leftpreferred eye (BEVLEF), the squint decreased instantaneously (to16.8±1.7 deg, i.e. 29 prism diopters). Saccades were still disconjugate,but their disconjugacy was systematically divergent followed by con-vergent postsaccadic drift. This pattern of disconjugacy (divergent in-trasaccadic disconjugacy followed by convergent postsaccadic drift)was qualitatively similar to that observed in normal subjects (see Col-lewijn et al.,10 Kapoula et al.,11 Zee et al.12), but is larger in amplitude(see below).
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119Attention and saccade coordination in strabismus
Quantitative data Squint measure. Figure 2 shows the average valueof squint averaged during the two minutes of each of the five condi-tions. For each condition, the three measures of the squint (at the be-ginning, at the end, and after the saccade) are presented. All threemeasures of squint are statistically smaller in the BEV natural condi-tion than in the other conditions (t-test comparing each mean in theBEV condition with the corresponding means in the other condition).When the subject was instructed to fixate attentionally with the lefteye, the squint measures were smaller than when she fixated attention-ally with the right eye (BEVREF versus BEVLEF). When one eye wascovered, the amount of squint was larger than when both eyes wereviewing. The difference of squint between the REV and BEVREFis statistically significant (t-test at P<0.05); similarly, the squint in theLEV condition is statistically significantly larger than in the conditionBEVLEF. From the four conditions manipulating the fixating eye, thesmallest squint and the closest to natural binocular viewing (BEV) wasproduced in the condition BEVLEF.
In summary, our objective measures of squint show large instanta-neous changes depending both on binocular stimulation and on theattentional effort of the subject to fixate with one or the other eye.Squint was smaller when the preferred eye was used for fixation rela-tive to the conditions where the nonpreferred eye was fixating, regard-
Fig. 1. Binocular recordings ofhorizontal saccades under threebinocular viewing conditions: (BEV)natural binocular viewing withoutinstruction; (BEVREF) viewing isbinocular, but the subject is instructedto fixate with the right nonpreferredeye; and (BEVLEF) binocularviewing with instruction to fixate withthe left eye. The solid and the dottedlines are the position trace of the leftand right eye, respectively. Saccadesto the right have positive direction.The thick line is the average of the twoeyes (LE+RE/2) – the cyclopean eye.The lower trace in each graphindicates the disconjugacy trace (LE-RE); it shows the squint angle duringand after the saccades. Fixatingattentionally with the right eyeincreases the squint even though botheyes are viewing.
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Fig. 2. Individual means of the squintangle measured during each of the fiveconditions at the beginning of thesaccade (white hatched bars), at theend of the saccades (white bar), and600 msec after the end of the saccade(black bar). Means are based on 34-70saccades. Leftward and rightwardsaccades are grouped together. *indicates a significant difference fromthe BEV condition (t-test significant atP>0.05); + indicates a significantdifference from BEVREF condition; ×indicates a significant difference fromthe REV condition; o indicates asignificant difference from the valueof the squint recorded at the beginningof the saccade in the same condition.(t-test significant at the level ofP>0.05.
less of the viewing condition. Are the changes in the squint accompa-nied by changes in binocular coordination of saccades?
Saccade yoking. Figure 3 shows the average amplitude (absolute value)of the disconjugacy of the rapid pulse component of the saccades (Fig.3A) and the averaged amplitude of disconjugate postsaccadic eye drift(Fig. 3B) in each of the five conditions. The amplitude of the discon-jugacy of saccades was remarkably variable for all testing conditions.The only significant difference between any two viewing conditionswas that between the two monocular viewing conditions (Fig. 3A).Postsaccadic drift was significantly larger in the condition REV than inthe BEV or the LEV condition.
In summary, the yoking of horizontal saccades is poor and variablein all conditions. The amplitude of disconjugacy does not show a con-sistent dependency upon the viewing or the fixating eye. Recall thateven in normal subjects the yoking of the saccades is not perfect andthe small normal disconjugacy is consistently divergent. We examinedwhether a similar pattern existed in this patient. The results are shownin Figure 4. In the condition BEV, the majority of the saccades hadconvergent disconjugacy just as found in a prior study.1 In contrast, inthe conditions manipulating the fixating eye explicitly, the majority ofsaccades showed divergent disconjugacy. The largest numbers of sac-cades with divergent disconjugacy occurred in the BEVLEF and LEVconditions where the subject used the preferred eye to fixate. The in-creased number of saccades with divergent disconjugacy was accompa-nied by an increase in the number of saccades followed by convergentpostsaccadic drift (see Fig. 4B, BEVREF, REV, and LEV conditionsversus BEV condition). In other words, attentional manipulation of thefixating eye brought about qualitatively the same stereotyped pattern ofdivergent intrasaccadic disconjugacy-convergent postsaccadic drift that
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121Attention and saccade coordination in strabismus
is observed in normal subjects. Even though the degree of yoking ofthe saccades remained poor when compared to normals, the disconju-gacy became as stereotyped as it is in normals. The immediate advan-tage of the systematically divergent disconjugacy was to reduce theangle of the squint at the end of the saccade. This is shown in Figure2: the measure of the squint was significantly smaller at the end of thesaccades than at the beginning of the saccades for the conditions wherethe left eye was fixating (BEVLEF or LEV).
binocular coordination of vertical gaze Figure 5 shows aseries of vertical saccades made by the patient under the three viewingconditions. In all of these conditions, the right eye was hypodeviatedby about 5 degrees, as shown by the disconjugacy trace. The maindifference between conditions was in the transient disconjugacy pro-duced by the saccade rather than in the steady-state squint. Several ofthe vertical saccades were unyoked in the REV condition; in the other
Fig. 3. Bars indicate in degrees theindividual mean values and standarddeviations of (A) the amplitude ofintrasaccadic disconjugacy and (B) theamplitude of postsaccadic driftdisconjugacy for each of the fiveviewing conditions. Means are basedon 34-70 saccades. Leftward andrightward saccades are groupedtogether. * indicates a significantdifference from the BEV condition; +indicates a significant differencebetween the REV and the LEVcondition (t-test comparing the meanssignificant at P<0.05).
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two conditions, the unyoking of the saccades was either smaller (BEV)or less frequent (LEV condition).
Quantitative data Squint measure. As for horizontal gaze, the verticalsquint was measured at three different times: at the beginning, at theend of the saccades, and 600 msec after the saccade. The vertical squintwas smaller than the horizontal and did not change significantly underthe three conditions. For instance, the mean value of squint measured600 msec after the end of saccades made during the 2-min period oftesting was: 5.8±0.9 deg (standard deviation, n=50) for the BEV con-dition, 4.9±0.4 deg (n=45) for the REV condition, and 6.5±0.4 deg(n=55) for the LEV condition.
Saccade yoking. Under BEV, the disconjugacy of the saccades wasvery small 0.13±0.72 deg (n=50) comparable to that known for normals(see Kapoula et al.4, Collewijn et al.,13 and Lemij14). In the two monoc-ular viewing conditions, the disconjugacy was significantly larger:0.71±0.44 deg (n=45) when the nonpreferred eye was viewing and
Fig. 4. Bars indicate (A) thepercentage of saccades with divergentdisconjugacy and (B) the percentageof saccades with convergentdisconjugate postsaccadic drift foreach of the five viewing conditionstested. Bars are based on 34-70saccades. Leftward and rightwardsaccades are grouped together.
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123Attention and saccade coordination in strabismus
0.37±0.50 deg (n=55) when the preferred eye was viewing. The discon-jugacy of the postsaccadic drift was slightly larger than that known innormal subjects in the LEV condition: 0.28±0.18 deg (n=55); Kapoulaet al.15 reported a disconjugate drift of only about 0.1 deg after verticalsaccades (for saccades of 15 deg of amplitude). In contrast, the valueof the disconjugate drift in the REV condition and in the BEV condi-tion was normal (0.19±0.13 deg, n=45 and 0.11±0.22 deg, n=50 respec-tively).
In conclusion, the vertical squint in this patient was mild and did notdepend on the viewing conditions. Yoking of vertical saccades wasalmost normal under BEV. Under monocular viewing the vertical bin-ocular motor control was slightly impaired, particularly when she viewedwith the nonpreferred eye. However, the unyoking of vertical saccadeswas still close to normal. Thus, binocular motor coordination in thevertical direction was mildly affected in this patient with primarilyconvergent strabismus.
Fig. 5. Binocular recordings ofvertical saccades under the threeviewing conditions: binocular viewing(BEV) and the two monocularviewings, right eye viewing (REV)and left eye viewing (LEV). Thesquint is indicated by the disconjugacytrace (LE-RE). Positive valuesindicate that the right eye ishypodeviated. Other notations as inFigure 1.
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exposure to optical aniseikonia: attempt to modify thecoordination of saccades Normal subjects are capable of chang-ing the natural binocular coordination of their saccades when they areexposed to image-size inequality (optically induced aniseikonia). Theirsaccades become rapidly larger in the eye that is viewing the largerimage. This inequality persists under subsequent monocular viewing,which indicates a fast learning mechanism.16 Kapoula et al.17 and Bucciet al.18 have reported the existence of such an ability in subjects withsmall or intermediate convergent strabismus, but failure in subjectswith large strabismus (>20 prism diopters).
We tested the ability of the patient to modify her motor coordinationby exposing her to image size inequality for 15 min. The paradigmused was similar to that used before.16 Briefly, a dichoptic viewingsetup based on polarizers provided an image to each eye: a random-dotpattern (33x33 deg) that was made 10% larger for the left preferredeye. Three conditions were used: a) the right eye pattern was coveredand the patient made horizontal and vertical saccades (of about 9 deg)between different points of the pattern that were indicated by the ex-perimenter; b) the patient looked binocularly, but dichoptically theunequally sized patterns and performed saccades to the same points;and c) the monocular viewing condition was repeated again. The con-dition (b) was called the training period and lasted about 15 min; con-ditions (a) and (c) were called pre- and posttraining, respectively, andlasted only 2 min each. During training, the binocular coordination ofhorizontal and vertical saccades remained unaffected by viewing theunequal patterns. The pretraining changes were very small and not sig-nificantly different (except for the postsaccadic drift after vertical sac-cades). The change of the intrasaccadic disconjugacy and the change ofthe disconjugacy of the postsaccadic drift for horizontal saccades were0.33±0.27 deg and 0.03±0.12 deg (n=182), respectively; the changesfor vertical saccades were -0.02±0.14 deg and 0.04±0.02 deg, (n=169).The pre-posttraining change of the disconjugacy of horizontal saccadeswas -1.19±0.29 deg and the change of the disconjugacy of the post-saccadic drift was -0.35±0.12 deg, (n=65). Both these changes werestatistically significant but in the wrong direction: i.e. saccades becamelarger in the right eye or this eye developed more onward drift. Forvertical saccades, a small but significant change in the good directionwas observed only for intrasaccadic disconjugacy: 0.14±0.05 deg (n=56).In summary, in agreement with our prior study,18 this experiment showsfailure in patients to learn to produce larger saccades in the eye view-ing a larger image.
Discussion The squint in this patient depended strongly on thefixating eye. Any form of binocular visual linkage was absent. Thepatient was diagnosed for ‘horror fusionis’ since childhood. At the timeof our examination, the patient could not even tolerate spectacle correc-tion and rejected any type of manipulation of binocular visual informa-tion. The strong incomitancy of the strabismus of this patient was cor-roborated by objective eye movement recordings. The most importantfinding is that the squint can change instantaneously by changing atten-tionally the fixating eye even though both eyes are viewing.
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125Attention and saccade coordination in strabismus
Another important new finding is that the instantaneous change in thesquint angle caused by attentional change of the fixating eye while botheyes were viewing translated to instantaneous changes in the quality ofbinocular coordination of saccades. The amplitude of the disconjugacyof horizontal saccades did not change significantly, but the disconjuga-cy became more systematically divergent as observed in normal sub-jects.4,10,11 The divergent disconjugacy of the saccades resulted in adecrease in the convergent squint at the end of the saccades and thiscan be seen as a form of improvement (see Fig. 2). In particular, thestereotyped nature of the disconjugacy of saccades when the subjectfixates with the preferred eye brought the eyes to a steretyped lessconvergent position. This could make the binocular stimulation of thetwo visual peripheries more likely.
It has been suggested that in normals the divergent transient saccadedisconjugacy is due to muscular mechanical differences (transfer func-tions or delays between the medial and lateral rectus (e.g., Zee et al.,12
Maxwell and King19). The observations in our patient strongly argueagainst a purely muscular explanation, because the pattern changesinstantaneously depended on the eye used attentionally for fixation andon the viewing conditions. Disconjugacy in our patient could be a de-liberate strategy for divergence during a saccade, just as suggested fornormal subjects by Collewijn et al.20
Between the two conditions where the left preferred eye was fixating(BEVLEF and LEV), it was the condition BEVLEF which producedthe most stereotyped pattern of divergent saccade disconjugacy andthus the smallest squint angle at the end of the saccade. This observa-tion suggests that binocular motor control in this patient, although driv-en by monocular visual inputs from the preferred eye (see comparisonREV versus LEV, Fig. 4, and for squint, Fig. 2), could still benefitfrom binocular visual stimulation. In that respect, our findings are inagreement with the study of Maxwell and King19 on amblyopic persons.Monocular visual inputs from the preferred eye seem to be more effi-ciently used when the other eye is also visually stimulated.
The third new finding of this study is that yoking of vertical saccadesis only mildly affected in this patient with large convergent strabismus.Recall that a non-negligible hypodeviation of 12 prism diopters, i.e.,56.8 deg, was also present. Yet, vertical binocular motor control wasalmost normal at least in the BEV condition. Our observations areconsistent with the idea that yoking of vertical saccades and Hering’slaw obedience is more hardwired than that of horizontal saccades (seeMoschovakis et al.21). Because of time limitations, we did not testwhether the attentional change of the fixating eye under binocular view-ing had any effect on the quality of vertical coordination.
Finally, the present study confirms a prior report18 that, in the case ofextreme strabismus, the ability of the subject to respond appropriatelyto the disparity induced by optical aniseikonia is diminished or inexis-tent. Such ability exists only when some binocular sensory coordina-tion, even rudimentary, exists and this was not the case in our patient.The observation of some modification in the vertical direction wasweak and inconclusive.
In summary, the oculomotor testing of this special patient sheds new
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light on the role of monocular visual input from the preferred eye in thequality of binocular motor coordination and also on the role of atten-tional influences. The results are compatible with the idea that visualinput from the preferred eye in the presence of some stimulation fromthe other eye constitutes a lower rudimentary form of ‘binocular vision’under which the squint angle is smaller and saccades present a stereo-typed pattern of discoordination qualitatively similar to that of normalsubjects.
References1 Kapoula Z, Bucci MP, Eggert T,
Garraud L. Impairment of thebinocular coordination of saccades instrabismus. Vision Res 1997;37:2757-2766.
2 De Faber JT, Van Rijn LJ, CollewijnH. Dynamics of saccades instrabismus and amblyopia. In:Kauffmann H, editor. Transactions ofthe 21st European StrabismologicalAssociation. Buren, The Netherlands:Æolus Press, 1994; 303-307.
3 Maxwell GF, Lemij HG, Collewijn H.Conjugacy of saccades in deepamblyopia. Invest Ophthalmol VisualSci 1995;36:2514-2522.
4 Kapoula Z, Hain TC, Zee DS,Robinson DA. Adaptive changes inpost-saccadic drift induced bypatching one eye. Vision Res 1987;27:1299-1307.
5 Bielschowsky A. Lectures on MotorAnomalies. Hanover, NH: DartmouthCollege Publications, 1956.
6 Von Noorden GK. Binocular Visionand Ocular Motility. Theory andManagement of Strabismus, 5th ed. St.Louis, MO: Mosby, 1996.
7 Kapoula Z, Bucci MP, Eggert T.Disconjugate adaptation of verticalsaccades in superior oblique palsy.Neuro-ophthalmology 1998;3:151-161.
8 Robinson DA. A method formeasuring eye movement using ascleral coil in a magnetic field. IEEETrans Biomed Eng 1963;10:137-145.
9 Collewijn H, Van der Mark F, JansenTC. Precise recordings of human eyemovements. Vision Res 1975;15:447-450.
10 Collewijn H, Erkelens CJ, SteinmannRM. Binocular coordination of humanhorizontal saccadic eye movements. JPhysiol 1988;404:157-182.
11 Kapoula Z, Robinson DA. Saccadicundershoot is not inevitable: saccadescan be accurate. Vision Res 1986;26:735-743.
12 Zee DS, Fitzgibbon EJ, Optican LM.Saccade-vergence interaction inhumans. J Neurophysiol 1992;68(5):1624-1641.
13 Collewijn H, Erkelens CJ, SteinmanRM. Binocular co-ordination ofhuman vertical saccadic eyemovements. J Physiol 1988;404:183-197.
14 Lemij HG. Asymmetrical adaptationof human saccades to anisometropicspectacles. PhD thesis, ErasmusUniversity, Rotterdam, theNetherlands, 1990.
15 Kapoula Z, Eggert T, Bucci MP.Disconjugate adaptation of the vertical
oculomotor system. Vision Res 1996;36:2735-2745.
16 Kapoula Z, Eggert T, Bucci MP.Immediate saccade amplitudedisconjugacy induced by unequalimages. Vision Res 1995;35:3505-3518.
17 Kapoula Z, Bucci MP, Eggert T,Zamfirescu F. Fast disconjugateadaptation of saccades inmicrotrabismic subjects. Vision Res1996;36:103-108.
18 Bucci MP, Kapoula Z, Eggert T,Garraud L. Deficiency of adaptivecontrol of the binocular coordinationof saccades in strabismus. Vision Res1997;37:2767-2777.
19 Maxwell JS, King WM. Dynamicsand efficacy of saccade-facilitatedvergence eye movements in monkey.J Neurophysiol 1992;68(4):1248-1260.
20 Collewijn H, Erkelens CJ, SteinmanRM. Voluntary binocular gaze-shiftin the plane of regard: dynamics ofversion and vergence. Vision Res1995;35:3335-3358.
21 Moschovakis AK, Scudder CA,Highstein SM. The microscopicanatomy and physiology of themammalian saccadic system. ProgrNeurobiol 1996;50:133-254.
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