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British Journal of Ophthalmology, 1986, 70, 673-676
Suppression and retinal correspondence inintermittent exotropiaJEFFREY COOPER AND CAROL DIBBLE RECORDFrom the Institute of Vision Research, SUNYIState College of Optometry, 100 East 24th Street, New York,New York 10010, USA
SUMMARY Suppression scotomas and retinal projection (retinal correspondence) were measuredin six intermittent exotropes during deviation. Measurements used red-green anaglyph stimulipresented on a black background which could be varied from 3-4 minutes of arc to 3024'. Resultsshowed non-suppression of all points between the fovea and the diplopia point. Harmoniousanomalous retinal correspondence was usually observed. Two subjects had spontaneous changesfrom anomalous retinal correspondence to normal retinal correspondence without a concurrentchange in ocular position. Conventional testing resulted in more variable results in regard to retinalcorrespondence and suppression, suggesting that non-suppression and anomalous retinal corres-pondence occur when black backgrounds are used for testing.
Patients with intermittent exotropia of the diverg-ence excess type (DE) or basic exotropia usually donot complain of diplopia when their eyes are deviat-ing.' Parks2 believes that the absence of diplopia isdue to a dense temporal hemiretinal suppression.Using a technique employing Risley prisms,Jampolsky3 demonstrated that DE patients have asuppression scotoma extending from the fovea to thepoint on the retina of the deviating eye which projectsto the object of regard (point zero or diplopia point).Travers4 and Pratt-Johnson and Wee' measureddense suppression scotomas at the fovea and pointzero of the deviating eye in intermittent exotropes.Awaya et al.' measured suppression at the fovea andpoint zero in 11 of 25 of the intermittent exotropesthat they tested, while using first degree targetprojected on a light fusional background.The clinically accepted convention is that
exotropes have a dense suppression in the deviatingeye. There is, however, evidence suggesting thatintermittent exotropes do not always suppress thedeviating eye. First, DE patients can often experi-ence diplopia when a red lens is placed over thefixating eye, while viewing a muscle light in adarkened room. Secondly, Cooper and Feldman7have demonstrated non-suppression of the fovea inthe deviating eye of DE patients. Thirdly, DEpatients often have non-suppression of the after-Correspondence to Jeffrey Cooper, OD.
image and anomalous retinal correspondence (ARC)in the deviated position and normal retinal corres-pondence (NRC) in the aligned position on theHering-Bielschowsky afterimage test.'We therefore attempted to qualify the depth of
suppression in deviating intermittent exotropes whilemonitoring ocular position. We used variable firstdegree anaglyph targets to measure suppressionscotomas. In the event of suppression we attemptedto break the suppression and measure the retinalcorrespondence between point zero and the fovea ofthe deviating eye.
Subjects and methods
There were six subjects, four were female and twomale. All had intermittent exotropia as measured bya distance and near cover test. Each was capable ofperforming in a restrained head apparatus and couldgive valid and reliable responses. They all had visualacuities correctable to at least 20/20 in each eye andcould perceive at least 40 arc seconds of stereopsis onthe Randot stereo test when binocularly aligned.
APPARATUSAn Atari 800 personal computer was used to presentanaglyph stimuli on a Sony 19-inch (48-cm) ColorMonitor.' The patient was seated 40 cm from themonitor and wore Keystone red-green glasses. The
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Jeffrey Cooperand Carol Dibble Record
red lens was in front of the habitually fixating eye.The monitor displayed a red cross, which subtendedan angle of 20; each line of the cross had a width of 3 9minutes of arc. The cross, viewed by the normallyfixating eye, had a mean luminance of 2 cd/M2.The second target was a green movable square orrectangle which also had a mean luminance of2 cd/M2. The green target could be instantly changedfrom a single-dot pixel (3-4 minutes of arc) to a 60-dotby 30-dot horizontal rectangle. The maximum greenshape subtended an angle of (3° 24'x 1° 42') to thepatient. The green target was movable so as tomeasure suppression areas. The background wasblack. The red and green targets were such that thered target could be seen only by the eye wearing thered filter and the green target by the eye wearing thegreen filter. Eye movements were monitored with aBiotronics Infrared Eye system combined with anauditory biofeedback apparatus. Thus the examinerwas assured of stable deviation or alignment duringtesting. Ocular movements more than 10 from the
green fIItr
present position (i.e., alignment or measured devia-tion position) resulted in an auditory tone (Fig. 1).
METHODSThe following conventional clinical tests were per-formed: Randot stereo test; troposcope evaluation ofsubjective and objective angles with a 1° target;Hering-Bielschowsky afterimage test; Bagolinistriated lens test; and a red lens test for diplopia. Allafterimage testing, Bagolini lens tests, and red lenstests were done in a darkened room. All ARC testingwas done in both the aligned and deviated position.
Suppression areas and retinal correspondencewere measured and recorded with the Atari 800microcomputer and a colour TV monitor. Thepatient fixated the red cross while the examinermoved the green target. Initially the examiner deter-mined the objective angle of deviation by means ofocclusion (i.e., cover test). The green target wasmoved until no movement on the cover test wasobserved. The eye movement apparatus was then
Os
Fig. 1 Patient is a right exotrope wearing red-green anaglyph glasses and infrared eye movementglasses. While viewing acolour monitor 40cm away thepatientfixates a red cross (+) with the OSand the examiner moves green box (-) seen by theOD. Examinermay control stimulus size with controller marked S; movestimulus with M; ormove thefixation target with F.FR is thefovea ofthe OD; FL is thefovea ofthe OS; andO ispoint zero orthe diplopiapoint. Ocularposition during binocularperimetric evaluation is monitored with Biotronics eye movement monitorsystem.
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Suppression and retinal correspondence in intermittent exotropia
calibrated so that, when the left eye moved from itsposition, a tone was triggered, and when the right eyedeviated a click was heard. The patient was thenasked to describe the relative position of the red andgreen targets. He/she was also asked to report ifeither the red or green targets disappeared. Theexaminer then moved the green target until thepatient reported superimposition (i.e., subjectiveangle).The green target was moved through the visual
field; the patient was asked to report any disappear-ance of either target. If the green target disappeared,the examiner used standard perimetric techniques tomap out the scotoma. Larger targets were producedto determine the density of the suppression scotoma.Plots were done horizontally, vertically, andobliquely. Randomly placed points were also pre-sented to pick up small scotomas and to verifykinetically determined retinal projection. Suppres-sion areas were recorded by the examiner by depress-ing a button on the joystick controller.
Periodically during testing the patient was asked topoint to either the fixation or the test target and to tellthe examiner if either target ever disappeared. Thepatient was also asked to describe the relative positionof each target. The examiner used 'catch trials' byextinguishing the stimulus to assure the validity of thepatient responses.
Results
Table 1 presents both experimental and orthopticfindings in the six intermittent exotropes tested. Fiveof the six subjects showed no suppressions duringexperimental testing, even with the smallest possibletarget. The sixth patient suppressed all size targetsthroughout experimental testing. Four of the non-suppressing patients gave ARC responses, with oneshowing NRC. Two of the ARC responders (nos. 1
Table 1 Orthoptic and experimentalfindings
DV NVPT CT CT TROPEXP BAG HBD HBA RL1 30 20 Sup NRC/ARC ARC ARC NRC Sup2 20 14 Sup HARC ARC NRC NRC Sup3 45 50 Sup NRC/ARC Sup NRC NRC Paradoxial dip4 57 59 NRC NRC NRC NRC NRC NRC5 25 18 Sup ARC Sup ARC NRC NRC6 50 12 Sup Sup Sup ARC NRC Sup
SUP=suppression. CT=prolonged cover test distance (DV) andnear (NV) in prism dioptres to obtain maximum deviation.TROP=troposcope findingsat the objective angle. EXP=red-greenanaglyph findings during experimental testing. BAG=Bagolini lensresults while an eye deviates. HBD=Hering-Bielschowsky testresults during deviation. HBA=Hering-Bielschowsky test resultsduring alignment. RL=red lens test results during deviation.
and 3) briefly changed from harmonious ARC toNRC without a concurrent change in ocular positionduring the course of testing. These two subjectsusually showed ARC. One patient (no. 4) showedNRC responses throughout testing and had thelargest deviation in the study on cover test.
Standard clinical testing yielded more variedresults. In the troposcope with first degree targets ona light background, five subjects suppressed com-pletely and one showed NRC. Bagolini striated lenstesting during deviation resulted in ARC responsesfor two subjects, NRC in one subject, and suppres-sion for the remaining three subjects. The Hering-Bielschowsky afterimage test performed in a dark-ened room yielded three cases of ARC and three ofNRC with no suppressions reported.
Discussion
Our results indicated the presence of non-suppres-sion of luminous targets in five of the six patientsacross the temporal portion of the retina duringexperimental testing. ARC was found during devia-tion and NRC during alignment. These findingssupport Morgan's motoric theory of ARC.'" How-ever, neither Burian's" adaptation theory norMorgan's theory are useful in explaining the instan-taneous changes in correspondence without a con-current change in ocular position observed in twopatients in this study and in a previous study.7The Hering-Bielschowsky and Bagolini lens tests
which are used to determine the presence of NRCwere done in a darkened room. The Hering-Bielschowsky test indirectly determines the presenceof foveal suppression in either eye, while the Bagolinitest indicates the presence of suppression at 'zeropoint'. It was shown that there was more suppressionon the Bagolini test than on the Hering-Bielschowskytest, indicating that the zero point (diplopia point) ofthe deviating eye suppresses more readily than thefovea of the deviating eye. The clinical observationthat it is more difficult to suppress the afterimages ofthe Hering-Bielschowsky test than the streaks of theBagolini test in a darkened environment was con-firmed by our study.Our findings are consistent with Jampolsky's
observation that not only size and brightness deter-mine the extent of suppression. We found that colourcomplexity of the stimulus and similarity of targetspresented to the two eyes may change suppressioncharacteristics. Only one patient suppressed duringour experimental procedure, which used differentcoloured stimuli on a black background. Pratt-Johnson and Wee- found both suppression of thefovea in the deviating eye and suppression of thedeviating eye at the point matched to the fovea of the
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fixating eye (zero point). We believe that Travers's4use of non-illuminated targets and Pratt-Johnson andWee's5 use of a white background triggered suppres-sions and resulted in findings different from ours.Awaya et al.6 used a phase difference haploscope
with and without a fusible background. Of the 11intermittent exotropes tested, who had a manifestdeviation during testing, nine showed suppression atpoint zero when a fusible background was present.Without a fusible background 15 showed suppres-sion of the deviating fovea, and the remaining 10showed superimposition at the objective angle. Theyconcluded that intermittent exotropes have suppres-sions with NRC. We did not find the consistency ofNRC nor the suppression that Awaya et al. reported.6These findings which differ from ours may beexplained by the observation of Jampolsky3 andGriffen'2 that differences in testing apparatus willalter suppression patterns.Our findings suggest that the intermittent exotrope
does not always suppress and usually has ARC underoptimal conditions, even with very small stimuli. Aspreviously stated, suppressions are dependent on thebackground. Black backgrounds seem to eliminatesuppressions, while light backgrounds result in activeinhibition or suppression. Our patients showed har-monious ARC, which extended from the point zeropast the fovea and through the entire nasal retina.Like suppressions, the ARC is liable to change undercertain test conditions. Retinal correspondencechanges with ocular position and occasionally with-out any change in stimuli or eye movements.These results may have important implications in
the orthoptic treatment of intermittent exotropia. Iftechniques can be employed which disrupt both theanomalous retinal correspondence mechanism andthe suppression mechanism, the DE patient will findit difficult to maintain deviation in the presence ofNRC diplopia. Sanflippo and Clahane,'3 Cooper,'and Awaya et al.6 have advocated diplopia awarenessand antisuppression therapy in the treatment ofintermittent exotropia. Our study suggests that oneshould start therapy with different coloured targetspresented to each eye with a darkened background.Therapy continues by gradually increasing theambient light and decreasing the filter intensity untilthe DE patient can experience NRC diplopia withoutthe use of filters in a fully illuminated room. In this
way one can be sure of breaking not only suppres-sions but ARC patterns as well.
In summary, our intermittent exotropes of the DEtype did not show suppressions even with very smalltargets (3-4 minutes of arc.) at either the fovea ordiplopia point of the deviating eye. Most of ourpatients showed harmonious ARC from the diplopiapoint to the fovea. Both suppression and retinalcorrespondence seem to change in accordance withstimuli, background, and retinal stimuli. Our results,which conflict with those of previous authors, areprobably explained by accurate control of ocularposition and use of a dark, non-fusible backgroundwith dissimilar targets. Our results suggest non-stability of a retinal correspondence (usually ARC)and non-suppression in the intermittent exotrope ofthe divergence excess type during deviation withsmall luminous targets on a dark background.References
1 Cooper J. Intermittent exotropia of the divergence excess type.JAm Optom Assoc 1977; 48: 1261-63.
2 Parks M. Concomitant exodeviations. In: Duane T, ed. Clinicalophthalmology. Philadelphia: Harper and Row, 1983; 1.
3 Jampolsky A. Characteristics of suppression in strabismus. ArchOphthalmol 1955; 54: 683-96.
4 Travers TB. Suppression of vision in squints and its associationwith retinal correspondence and amblyopia. Br J Ophthalmol1938; 22: 577-604.
5 Pratt-Johnson J, Wee HS. Suppression associated withexotropia. Can J Ophthalmol 1969; 4: 136-44.
6 Awaya S, Nozaki H, Itoh T, Kikuko H. Studies of suppression inalternating constant exotropia. In: Moore S, Mein S, Stock-bridge L, eds. Orthoptics: Past, Present and Future New York:Stratton Intercontinental: 1975.
7 Cooper J, Feldman J. Panoramic viewing, visual acuity of thedeviating eye and anomalous retinal correspondence in inter-mittent exotropia of the divergence excess type. Am J OptomPhysiol Opt 1979; 56: 422-9.
8 Bielschowsky A. Divergence excess. Arch Ophthalmol 1934; 12:157.
9 Cooper J, Citron M. Microcomputer produced anaglyphs forevaluaton and therapy of binocular anomalies. J Am OptomAssoc 1983; 54: 785-8.
10 Morgan MW. Anomalous correspondence interpreted as amotor phenomenon. AmJ Optom Physiol Opt. 1961; 38:131-48.
11 Burian HM. The sensorial retinal relationship in concomitantstrabismus. Arch Ophthalmol 1947; 37: 336-68.
12 Griffen JR. Binocular anomolies procedures for vision therapy(c) 1976. Chicago, Ill. p.46.
13 Sanflippo S, Clahane A. Effectiveness of orthoptics alone inselected cases of exodeviation: the immediate results and severalyears later. Am OrthoptJ 1970; 20: 104-17.
Acceptedforpublication 31 December 1985.
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doi: 10.1136/bjo.70.9.673 1986 70: 673-676Br J Ophthalmol
J Cooper and C D Record exotropia.correspondence in intermittent Suppression and retinal
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