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CHAPTER 13 Examination of the Patient—III SENSORY SIGNS, SYMPTOMS, AND BINOCULAR ADAPTATIONS IN STRABISMUS W hen a manifest deviation of the visual axes of the two eyes is present, images of all objects in the binocular field are shifted onto the retinas relative to each other; the larger the shift, the greater the deviation. Motor and sensory fu- sion may become impossible, with two distressing results. First, different objects are imaged on cor- responding areas (the two foveae) and therefore are seen in the same visual direction and overlap (Fig. 13–1A). Second, identical objects (the fixa- tion point) are imaged on disparate retinal areas (the fovea of one eye and the peripheral retina of the other eye) and therefore are seen in different visual directions; that is, they are seen double (Fig. 13–1B). The first phenomenon is termed confusion 96 ; the second, diplopia. Strictly speaking, confusion and diplopia are not abnormal. They are physiologically correct sensory responses. They must occur in every pa- tient who has adequate vision in each eye but in whom an acute relative deviation of the visual axes has developed. To avoid them, the visual system has at its disposal two mechanisms: sup- pression and anomalous correspondence. Another prominent sensory sign in comitant strabismus, 211 likely to be closely related to suppression, is am- blyopia. Suppression, amblyopia, and anomalous corre- spondence are ‘‘nature’s way out of trouble’’ for the patient who by these mechanisms gains com- fortable single monocular vision or an anomalous form of binocular cooperation. One may consider them to be adaptive sensory mechanisms by which the sensory system adjusts to an abnormal motor situation. This interpretation implies that the sen- sory responses are a consequence of the motor anomaly. In contrast, it has been stated that the sensory anomalies in strabismus may be present at birth, 1 heritable, 131, 154 and indeed the cause of a deviation. Evidence supporting this view is ex- tremely tenuous. Moreover, sensory anomalies can often be eliminated with treatment, another argu- ment in favor of the fact that these anomalies cannot be the cause of a deviation. However, it is true that there must be a predisposition to sensory anomalies; that is, a weakness in the sensory an- lage, more pronounced in families in which stra- bismus occurs in several members, and this weak- ness is possibly a heritable trait. 43 Thus some patients suppress very readily and others only with

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Page 1: 13 - Semantic Scholar · 2018-04-14 · CHAPTER 13 Examination of the Patient—III SENSORY SIGNS, SYMPTOMS, AND BINOCULAR ADAPTATIONS IN STRABISMUS When a manifest deviation of the

C H A P T E R 13Examination of thePatient—III

SENSORY SIGNS, SYMPTOMS, ANDBINOCULAR ADAPTATIONS INSTRABISMUS

When a manifest deviation of the visual axesof the two eyes is present, images of all

objects in the binocular field are shifted onto theretinas relative to each other; the larger the shift,the greater the deviation. Motor and sensory fu-sion may become impossible, with two distressingresults. First, different objects are imaged on cor-responding areas (the two foveae) and thereforeare seen in the same visual direction and overlap(Fig. 13–1A). Second, identical objects (the fixa-tion point) are imaged on disparate retinal areas(the fovea of one eye and the peripheral retina ofthe other eye) and therefore are seen in differentvisual directions; that is, they are seen double(Fig. 13–1B). The first phenomenon is termedconfusion96; the second, diplopia.

Strictly speaking, confusion and diplopia arenot abnormal. They are physiologically correctsensory responses. They must occur in every pa-tient who has adequate vision in each eye but inwhom an acute relative deviation of the visualaxes has developed. To avoid them, the visualsystem has at its disposal two mechanisms: sup-pression and anomalous correspondence. Anotherprominent sensory sign in comitant strabismus,

211

likely to be closely related to suppression, is am-blyopia.

Suppression, amblyopia, and anomalous corre-spondence are ‘‘nature’s way out of trouble’’ forthe patient who by these mechanisms gains com-fortable single monocular vision or an anomalousform of binocular cooperation. One may considerthem to be adaptive sensory mechanisms by whichthe sensory system adjusts to an abnormal motorsituation. This interpretation implies that the sen-sory responses are a consequence of the motoranomaly. In contrast, it has been stated that thesensory anomalies in strabismus may be presentat birth,1 heritable,131, 154 and indeed the cause of adeviation. Evidence supporting this view is ex-tremely tenuous. Moreover, sensory anomalies canoften be eliminated with treatment, another argu-ment in favor of the fact that these anomaliescannot be the cause of a deviation. However, it istrue that there must be a predisposition to sensoryanomalies; that is, a weakness in the sensory an-lage, more pronounced in families in which stra-bismus occurs in several members, and this weak-ness is possibly a heritable trait.43 Thus somepatients suppress very readily and others only with

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FIGURE 13–1. Effects of the relative deviation of the visual lines. A, Confusion. B, Diplopia. NRC,Normal retinal correspondence. (From Burian HM: Adaptive mechanisms. Trans Am Acad OphthalmolOtolaryngol 57:131, 1953.)

difficulty or not at all. In some, the angle ofanomaly (see p. 230) adapts almost instantane-ously to changed motor conditions; in others itremains unchanged over years and decades inspite of changes in the deviation. In adults, sup-pression, amblyopia, and changes in retinal corre-spondence do not occur. Hence in adults an ac-quired strabismus will cause constant diplopia. Onthe other hand, visually immature children usuallyadapt readily to strabismus and diplopia rarelybecomes a problem.

None of the abnormal sensory responses addanything qualitatively new to the act of vision. Allabnormal responses of squinters are preformed inthe normal act of vision and are perversions orexaggerations of it.33 Thus suppression and, byextension, amblyopia represent a loss of therhythm of binocular rivalry. Anomalous corre-spondence is an extreme shift in visual directionsthat occurs under physiologic conditions in stere-opsis (see Chapter 2).

Confusion and diplopia obviously occur onlywhen the patient uses both eyes, but suppressionand anomalous correspondence are also basicallybinocular phenomena. To be sure, suppressionmay be restricted to one eye, amblyopia may bean extreme form of such suppression, and mainte-nance of a shift in monocular visual directions,akin to anomalous correspondence, has beenclaimed to be responsible for eccentric fixationin amblyopia.50 The fact remains, however, thatexclusion of one eye from the act of vision sig-

nificantly affects depth of suppression in the othereye and even the functioning of amblyopic eyes.Suppression in one eye can be interrupted byreducing the stimulus to the other eye; the sizeand depth of the suppression scotoma depend onthe amount of stimulation to the other eye, as doesvisual acuity of the amblyopic eye.

The examination of the sensory state of a pa-tient with neuromuscular anomalies of the eyesconsists of establishing (1) the presence of confu-sion and diplopia, (2) the presence and degreeof suppression, (3) the presence and degree ofamblyopia, (4) the type of interocular relationshippresent (normal and anomalous correspondence),and (5) the patient’s responsiveness to disparateretinal stimulation (stereopsis).

Confusion and Diplopia

Confusion is not often reported voluntarily, butwhen patients do notice overlap of the differentfoveal images, they find it very distressing. Onthe other hand, diplopia is a common complaint.

When a patient has a complaint about doublevision or admits, when questioned, to seeing dou-ble, a methodical algorithmic approach (Fig. 13–2)is helpful in analyzing the problem, especiallywhen an obvious strabismus is not apparent duringthe initial examination. The ophthalmologist mustrealize that ‘‘double’’ vision means differentthings to different people. Blurred vision of one

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Examination of the Patient—III 213

FIGURE 13–2. Algorithmic approach to analyzing double vision. For explanation, see text. (Modifiedfrom Noorden GK von, Helveston EM: Strabismus: A Decision-Making Approach. St Louis, Mosby–Year Book, 1994, p 68.)

eye, an overlay of the image seen by both eyes,or a halo surrounding this image is often interpre-ted as double vision. Thus at the beginning of theexamination it must be established whether theimages are truly separated. We let the patient drawwhat is seen or hold a vertical prism before oneeye to demonstrate to the patient what true doublevision is like. Once it can be confirmed that diplo-pia is real, placing a cover over either eye willdetermine whether it is monocular or binocular incharacter. In the former case any further searchfor a neuromuscular anomaly of the eyes can besuspended.

Monocular Diplopia

Monocular diplopia may occur in one or in botheyes and is usually caused by anomalies of theocular media, in which case it will disappearreadily when the patient looks through a pinhole.The most common cause, in our experience, issubtle changes in optical density of the anteriorand posterior layers of the lens in certain cases ofincipient cataracts, which can only be appreciatedafter pupillary dilation and with a narrow, obliqueslit beam. Because of the different refractive indi-ces of the lens layers in such eyes, a parallel

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bundle of light is not refracted uniformly but atdifferent angles so that two or more retinal pointsreceive the same image (polyopia). Occasionally,monocular diplopia may be caused for opticalreasons by anomalies of the tear film, the cornea,the vitreous, a dislodged pseudophakos, or ordi-nary refractive errors.48 An unusual case of mon-ocular diplopia caused by pressure of the upperlid on the cornea was reported by Kommerell.95

Monocular diplopia of sensory origin occursinfrequently and will persist even when viewingthrough a pinhole. It is sometimes observed afterbrain trauma or a cerebrovascular accident, inwhich case the patient usually becomes aware ofmore than two images seen with one eye (poly-opia). It may also occur during treatment of am-blyopia or, transiently, in a deeply amblyopic pa-tient after loss of the sound eye.

Binocular Diplopia

When diplopia is binocular, a red filter held beforeone eye will determine whether it is uncrossed(or homonymous), in which case an esotropia ispresent; crossed (or heteronymous), in which casethe patient has exotropia; or vertical, in whichcase hypertropia or hypotropia is present; or tor-sional in the case of cyclotropia. If diplopia occursafter surgery, it must be determined whether it isin accordance with the postoperative deviation orparadoxical (crossed with esotropia or uncrossedwith exotropia), in which case there is a persis-tence of the preoperative angle of anomaly (seep. 237).

If the diplopia is binocular, one must determinethe frequency of its occurrence, whether it is con-stant or transient, and whether the distance be-tween the images increases or decreases in differ-ent directions of gaze and with different headpositions. Information on these points is helpfulin making a presumptive diagnosis. Confusion be-tween the two competing images often becomesthe most disturbing problem for the patient. Thedecision which of the two visual objects to fixateis probably related to the attention value of eachobject. The diplopia pattern is the subjective corre-late of the prism and cover test. When the sensoryrelationship between the eyes is normal, the rela-tive position of the two images is a measure ofthe deviation. Application of the diplopia methodsfor determination of the amount of the deviationis described in Chapter 12.

Spontaneous diplopia, though always present in

adults with recently acquired extraocular muscleparalysis, is by no means the rule in all patientswith neuromuscular anomalies of the eyes. In pa-tients with congenital paralytic strabismus or com-itant deviations, spontaneous diplopia is rare andusually the result of a spontaneous surgical changeof the angle of strabismus that causes the imagein the deviated eyes to fall outside of a previouslyestablished suppression scotoma. Other causes in-clude a switch in fixation preference in strabismicpatients who do not alternate spontaneously. Thiscondition was defined as fixation switch diplopia.26

Its pathogenesis can be sought in an asymmetryof the depth of the suppression scotomas in nonal-ternating strabismus; the potential for suppressionis weaker in the habitually preferred eye. There-fore, the patient experiences diplopia when theusually deviated eye takes up fixation. This canhappen in anisometropia, when fixation switchesfrom an eye with incipient myopia to the lessmyopic or hypermetropic fellow eye.130 Correctionof the myopia will quickly resolve this problem.Even changes in the refractive correction of spec-tacles lenses can cause this phenomenon.97

Another cause of sudden awareness of diplopiain strabismus of long standing is a change inthe angle of anomaly or normalization of retinalcorrespondence after surgery or prolonged alter-nating occlusion.146

An unusual and intriguing form of binoculardiplopia occurs in the absence of manifest strabis-mus or a history of such and in association withsubretinal neovascular membranes28 or retinalwrinkling.21 Because of retinal traction the fovealphotoreceptors become disarranged with respectto the retinal periphery. While peripheral fusion ismaintained, such patients may experience meta-morphopsia or diplopia with both eyes open. It hasbeen suggested that this phenomenon is caused byan induced fixation disparity.152 Special diagnosticslides for the synoptophore have been developedfor such patients to compare superimposition offoveal targets simultaneously with peripheral tar-gets77 and a partially occlusive Bangerter foil overthe affected eye may give relief from diplopia.28

Spontaneous diplopia has also been associatedwith aniseikonia from separation or compressionof photoreceptors in patients with epiretinal mem-branes or vitreomacular traction. An incorrect di-agnosis of central disruption of motor fusion (seeChapter 21) could be erroneously made in suchcases.16

Binocular diplopia in the absence of stabismus

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Examination of the Patient—III 215

or a history of such that is eliminated by coveringone eye may be caused by awareness of physio-logic diplopia (see Chapter 2). In such cases wetry to explain this phenomenon and to reassurethe patient.

Binocular triplopia, a combination of monocu-lar and binocular diplopia, is discussed on page238.

Suppression

Diplopia is most repugnant, and persons so af-fected make every effort to avoid it. Whereverpossible the images are brought together by motorfusion, even at the expense of muscular astheno-pia. In some patients an abnormal head positionis assumed in which the distance between thetwo images is minimized (see Chapter 12). Whenfusion is not possible and the patient is a child,suppression may develop to eliminate double vi-sion. Suppression may be defined as the activecentral inhibition of disparate and confusing im-ages originating from the retina of the deviatedeye. Since there is no need to suppress whendouble vision is eliminated by closing one eye,suppression is strictly limited to binocular vision.

Mechanism and Seat

Binocular rivalry is basic to binocular vision (seeChapter 2), but disappears in patients with strabis-mus. Only images received by one eye can enterconsciousness. Suppression may be alternating orstrictly monocular, depending on the type of fixa-tion used by the patient.

The mechanism and seat of rivalry and suppres-sion in abnormal binocular vision have been ex-tensively studied. Burian’s concept that suppres-sion is merely an exaggeration of the same processinvolved in blocking out certain parts of the imageseen by each eye in binocular rivalry was chal-lenged by Smith and coworkers.151 These authorsfound that binocular rivalry differentially attenu-ates chromatic mechanisms relative to luminancemechanisms. In contrast, strabismic subjects didnot manifest wavelength-specific sensitivity loss.Smith and coworkers concluded that suppressionand normal binocular rivalry are mediated by dif-ferent neural processes, but conceded that rivalrymay be an important phase in the development ofstrabismic suppression. It must be noted that thestrabismic subjects examined by Smith and co-

workers also had mild degrees of amblyopia andit remains to be shown that the same findings canbe obtained in suppression uncontaminated by acoexisting amblyopia, that is, in true alternators.More recent neurophysiologic work has substanti-ated Burian’s original concept about the relation-ship between retinal rivalry and suppression byshowing the similarity of interocular suppressionin strabismic cats vs. normal cats that were pre-sented with conflicting visual stimuli.142–144 Quiterecently, this subject was analyzed again by Har-rad,72 who also considered binocular rivalry to bethe basis for suppression. Another argument infavor of Burian’s concept is the fact that the differ-ent time courses of suppression and rivalry can beeliminated. Artificial attenuation of the dominanteye in strabismic amblyopia produces time coursesof suppression which are similar to those of nor-mal observers.53, 147

Barany and Hallden15 demonstrated that in bin-ocular rivalry the threshold of pupillomotor re-sponses is higher during the suppression phasethan when the eye is perceiving. These resultswere not confirmed by Lowe and Ogle,104 butBrenner and coworkers27 found the pupillomotorresponse to be greater when the fixating eye isstimulated than when the suppressed or amblyopiceye is stimulated. The difference in effect wassmall in binocular rivalry; it increased in magni-tude as suppression and amblyopia deepened.

Responses of the visual cortex to photic stimuli(visual evoked responses, VERs) also have beenrecorded during retinal rivalry. Some authors37, 91,

99, 100, 163 found the amplitude to be reduced duringthe suppressed phase, but others47, 132 found nochange.

Franceschetti and Burian58 studied VERs in pa-tients with alternating esotropia. In each instancethey found that considerably larger amplitudeswere present when the fixating eye was stimulatedthan when the nonfixating eye was stimulated.The effect reversed with alternation of fixation.

Differences in the VER recorded during rivalryand with suppression leave no doubt that corticalcells participate in the mechanism responsible forthese phenomena. Blake and Lehmkuhle22 pre-sented additional evidence for this view. Theyshowed that a grating pattern presented to oneeye of a patient who is capable of alternatingsuppression induces a visual aftereffect (contrastthreshold elevation), even when the pattern is sup-pressed while being viewed by the patient. Thisfinding seems to indicate that suppression occurs

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216 Introduction to Neuromuscular Anomalies of the Eyes

within the visual system beyond the site of theaftereffect.

A reduction in pupillomotor sensitivity of thesuppressed eye, if definitely established, however,might favor retinal involvement in suppression. Afinal answer to the question of the primary seatof the suppressive mechanism is not available atpresent, although most studies implicate the cor-tex. For example, van Balen159 simultaneously re-corded the electroretinogram (ERG) and the VERand found no reduction in the ERG, even whenthe amplitude of the VER was reduced.

Compared with the wealth of clinical, psycho-physical, electrophysiologic, and even histologicinformation available on amblyopia it is discon-certing how little corresponding information hasbeen collected on suppression. Most electrophysi-ologic and psychophysical evidence places theseat of suppression in the visual cortex. This viewis supported by the findings of Sengspiel andcoworkers144 who recorded from cortical neuronsin cats with alternating eso- and exotropia andshowed that there is only minimal excitatory inputfrom the suppressed eye. These authors suggestedthat suppression may depend on inhibitory interac-tions between neighboring ocular dominance col-umns. Horton et al.82 recently reported results ob-tained by metabolic mapping of suppressionscotomas in the striate cortex of adult macaquesthat underwent a free tenotomy of both medialrectus muscles and developed an exotropia withstrong fixation preference for one eye. Autoradio-graphic labeling of the ocular dominance columnsin the striate cortex and cytochrome oxidase pro-cessing for assessment of local metabolic activityshowed such activity to be reduced in the deviatedeye’s monocular dominance columns and in thebinocular border strips. In two animals with aweak fixation preference, resembling alternatingfixation, anomalous staining was present withinthe central visual field representation in bothhemispheres. According to the authors, this is thefirst experimental demonstration of structural andmetabolic anomalies in association with suppres-sion in the striate cortex of primates. However,the authors did not test for suppression psycho-physically or electrophysiologically so that thepresence of suppression in these adult monkeys isonly inferred. Whether these findings are directlyapplicable to suppression in humans remains to beseen because the ability to develop suppressionin humans is limited to childhood and becausesuppression rarely occurs in paralytic, incomitant

strabismus where diplopia is avoided by an anom-alous head posture.

Crewther and Crewther49 had shown earlier instrabismic cats that active suppression of the re-sponse to monocular stimulation of the deviatedeye occurs when the fixating eye is simultaneouslystimulated. While these data support what can beobserved in patients with strabismus, it is still notclear by what process the visual system managesso effectively and within milliseconds to switchon and off selected information that reaches thecortex from the retina of either eye.

Clinical Features

In strabismus one eye is not excluded entirelyfrom vision in spite of the presence of suppres-sion. Most patients have some binocular coopera-tion, ranging from rudimentary to remarkably highforms of binocularity. Only in rare cases, particu-larly in exotropic patients with alternation, arethere two seemingly quite independent visual sys-tems with suppression of essentially the wholeof one retina. In all other patients, suppression isregional.

To avoid confusion and diplopia, suppressionmust occur in the fovea of the deviated eye andthat region in the periphery of the deviated eye onwhich the object of attention is imaged (fixationpoint scotoma70). Using some form of binocularperimetry, it can be shown that in the deviated eyethere are two functional scotomas correspondingto these areas70, 106 (Fig. 13–3). The greater thedeviation, the larger the extent of the second pe-ripheral scotoma. In some instances of very deepsuppression, the two scotomas may fuse into one.These scotomas are less frequently found whenthe testing conditions resemble those present un-der casual conditions of seeing.19, 32, 77 Indeed, ithas been suggested that they are artifacts, causedby binocular rivalry.94, 110 The fixation point sco-toma found so frequently in microtropia with theBagolini striated glass test12 (see Fig. 13–15C ) iscertainly not an artifact. Interestingly, the fovea ofthe deviated eye is not always suppressed in smallangle strabismus, even in the presence of moderateamblyopia. There may be a range of differentmanifestations of suppression: (1) antidiplopic andanticonfusion suppression scotomas and (2) onlyantidiplopic suppression scotoma (fixation pointscotoma).

In strabismic patients who strongly prefer oneeye for fixation, scotomas are always found in the

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Examination of the Patient—III 217

FIGURE 13–3. Peripheral fixation point and central sup-pression scotomas in deviated eye. (Modified from BurianHM: Adaptive mechanisms. Trans Am Acad OphthalmolOtolaryngol 57:131, 1953.)

fellow eye. In those patients who can be made tofixate with either eye and in those who alternatefreely, scotomas are found alternately in the righteye or the left, depending on fixation (Fig. 13–4).Steinbach153 determined that it takes less than 80ms to switch fixation and suppression from oneeye to the other in alternating exotropes.

Suppression scotomas are not limited to thedeviated eye. They can also be found in the fixat-ing eye near the fovea157 or in the periphery146

during stimulation of the fovea of the deviatedeye. Suppressed areas in the field of vision of one

FIGURE 13–4. Alternating foveal sup-pression. (From Burian HM: Adaptivemechanisms. Trans Am Acad Ophthal-mol Otolaryngol 57:131, 1953.)

eye may be complemented by a nonsuppressedportion from the field of vision of the other eye.

As with other types of sensorial adaptations,such as amblyopia and anomalous retinal corre-spondence (ARC), the ability to suppress is lim-ited to the immature visual system, that is, itdevelops only in children. Although no compara-tive studies exist, it is our clinical impression thatthe sensitive period during which suppression maydevelop ends after the age of 8 or 9 years; thus itis similar to the sensitive period for amblyopia.However, once developed, suppression may per-sist throughout life. If a patient loses the ability tosuppress during adulthood through head trauma,ill-advised orthoptic treatment, or surgical or spon-taneous change of the angle of strabismus, it cannever be regained and double vision prevails.

Tests for Suppression

Binocular Perimetry and Haploscopy

Binocular perimetry can be done with any type ofhaploscopic device that allows scanning of theretinas. For the clinician, the simplest means isthe use of one form of color differentiation, suchas red-green spectacles. If the left eye, providedwith a green filter, fixates a green spot and theright eye is provided with a red filter, a projectedred light will be seen everywhere by the right eyeexcept in the region of the scotomas. To test theleft eye, reverse the filters before the eyes. Onemay also use the system, introduced by Travers,157

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218 Introduction to Neuromuscular Anomalies of the Eyes

consisting of two tangent screens at right anglesto each other. The patient faces the screen in frontof him or her, the middle of which the patientfixates, say, with the left eye. The second screenis to the right. Before the right eye is a mirror soadjusted that it offsets the deviation. The centerof the second screen is then imaged on the fovea.While the patient fixates with the left eye, perime-ter targets are presented to the right eye and thescotomas are mapped out (Fig. 13–5).

When one interprets the results of clinical re-search on suppression, it is important to know thetesting conditions under which such data wereobtained. For instance, dissociation of the eyes bythe use of red-green spectacles introduces condi-tions different from those that prevail when theeyes are used under casual conditions. Polaroiddissociation or dissociation with the phase differ-ence haploscope of Aulhorn3 (see Chapter 4) pro-duces more natural conditions of seeing. UsingPolaroid methods, Pratt-Johnson and MacDon-ald128 (see also Herzau77) showed that suppressiondoes not exclusively involve the nasal retina inesotropes and the temporal retina in exotropesbut extends nasalward and templeward from thefixation point, regardless of the direction of thedeviation.

Similar findings were reported by Campos,38

who used the mirror-screen technique of Travers(see Fig. 13–5) and found that the suppressionscotoma in large angle exotropia often overridesthe vertical retinal meridian to extend into thenasal retina. In contrast, the same author, by using

FIGURE 13–5. Screen and mirror arrangement of Traversfor the mapping of suppression scotomas in strabismus.(From Burian HM: Adaptive mechanisms. Trans Am AcadOphthalmol Otolaryngol 57:131, 1953.)

a modified von Graefe’s technique for binocularvisual field examinations, found a hemianopic sco-toma with a dense red filter before the fixating eye(see Fig. 17–2). Thus it appears that the concept of‘‘hemiretinal suppression’’86 according to whichonly the temporal retina is suppressed in alternat-ing exotropia, can no longer be upheld when lessdissociating tests are being used.

When orthoptic instruments are available, thehaploscopic arrangement is provided by a majoramblyoscope with which the suppression scotomacan be mapped, at least in the horizontal meridian.One arm is rotated, and the points are noted atwhich the target carried by the moving arm disap-pears and reappears.

Prisms

In clinical practice, by using prisms one can esti-mate in a simple way the extent of a suppressionscotoma. The patient may not see double eitherspontaneously or with the addition of a red glassplaced in front of one eye. By placing prisms ofincreasing strength in front of the eye, one willsoon find a prism with which the patient reportsdiplopia. The image of the fixation point, prefera-bly a small light source, is now thrown out of theregion of the suppression scotoma onto a retinalarea that is not habitually suppressed. The powerand direction of the base of the prisms required toproduce diplopia is a measure of the extent of thesuppression scotoma (Fig. 13–6).

The Four-Prism Diopter Base-OutPrism Test

The four-prism diopter base-out prism test is ofsome value in determining whether a patient hasbifoveal (sensory) fusion or a small suppressionscotoma under binocular conditions or to assessthe quality of binocular vision in postoperativeorthotropes. This test was introduced by Irvine84

and popularized by Jampolsky87 and is illustratedin Figure 13–7.116 A four-prism diopter base-outprism is held before one eye while the patientfixates on a penlight and the observer notes thepresence or absence of a biphasic movement ofthe fellow eye (Fig. 13–7A,B). Several atypicalresponses to this test have become known, whichlimits its value as an objective screening devicefor the presence of foveal suppression.56, 59, 133, 137

This is especially so in microtropias where theprism held before the minimally deviated eye may

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Examination of the Patient—III 219

FIGURE 13–6. Measuring the size of a suppression sco-toma. A, Right esotropia causes the image of the visualobject fixated by the left eye (OS) to fall on nasal retinalelements of the deviated right eye (OD). Suppressioneliminates diplopia. B, Base-out prisms before OD areincreased until crossed diplopia occurs; the temporal bor-der of the scotoma has been defined. C, Base-in prismsbefore OD are increased until uncrossed diplopia occurs;the nasal border of the scotoma has been defined. Thetotal prismatic power required to move the image fromthe temporal to the nasal border of the scotoma indicatesthe horizontal diameter of the scotoma. The vertical ex-tent of the suppression scotoma can be determined in asimilar fashion. (From Noorden GK von: Atlas of Strabis-mus, ed 4. St Louis, Mosby–Year Book, 1983.)

merely shift the retinal image within an area ofabnormal binocular vision, maintained by abnor-mal retinal correspondence. The patient will expe-rience single binocular vision in spite of theshifted retinal image and without a corrective eyemovement.13 However, a biphasic movement re-sponse of either eye (see Fig. 13–7B) in an ortho-tropic patient after placing the prism before thefellow eye usually indicates bifoveal fusion, al-

though atypical responses may occur even in thiscondition.138

A foveal (central) suppression scotoma in or-thotropic patients or a fixation point scotoma inmicrotropes can also be detected with the striatedglasses test of Bagolini (p. 228). In the former thepatient will see a central interruption of the lightstreak at the crossing point. In the latter the inter-ruption will be off center in one streak. A Polaroidtest has been recently introduced for testing rap-idly and reliably the presence of a central suppres-sion scotoma.121 Yet, in the fixation area the stimu-lus is presented only to one eye at a time, thusfavoring retinal rivalry and hence suppression.Moreover, the position of the eyes is crucial aswith all tests based on the use of polarized filters.

Monocular Visual Acuity MeasuredUnder Binocular Conditions

A more effective test for foveal suppression inmicrotropias or in patients with subnormal binocu-lar vision after surgical correction of essentialinfantile esotropia (see Chapter 16) is to measurethe visual acuity of each eye under binocular con-ditions with the Project-O-Chart slide of AmericanOptical.137 A decrease of visual acuity of one eyethat is not present when the eye is tested undermonocular conditions will readily indicate fovealsuppression.

The Worth Four-Dot Test

Suppression involving the peripheral retina canalso be diagnosed with the widely used Worthfour-dot test (Fig. 13–8). In our opinion this testis only of limited value and therefore is rarelyused in our clinic. Among its disadvantages isthat the eyes are easily dissociated with red-greenspectacles. Thus a patient with unstable but func-tionally useful binocular vision may exhibit a sup-pression response when the Worth four-dot test isused. Another disadvantage is that the presence orabsence of bifoveal fusion cannot be assessed. Afusion response (the patient sees all four dots in arectangular arrangement) may occur in the pres-ence of heterotropia with ARC and may be misin-terpreted, as is frequently done in the literature, asevidence of normal binocular vision. It is all toooften neglected that this test becomes meaningfulonly when used in conjunction with the covertest.118

Arthur and Cake2 proposed a modification of

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FIGURE 13–7. The four-prism diopter base-out prism test. A, When a prism is placed over the lefteye, dextroversion occurs during refixation of that eye, indicating absence of foveal suppression inthe left eye. If a suppression scotoma is present in the left eye, there will be no movement of eithereye when placing the prism before the left eye. B, A subsequent slow fusional adduction movementof the right eye is observed, indicating absence of foveal suppression in the right eye. C, In a secondpatient the right eye stays abducted, and the absence of an adduction movement (B) indicates fovealsuppression in the right eye or anomalous retinal correspondence. D, Another cause for absence ofthe adduction movement is weak fusion, and such patients will experience diplopia until refusionoccurs spontaneously. (From Noorden GK von: Present status of sensory testing in strabismus. InSymposium on Strabismus: Transactions of the New Orleans Academy of Ophthalmology. St Louis,Mosby–Year Book, 1978, p 51.)

the Worth four-dot test, in which the differentia-tion of the stimuli for the two eyes is obtainedwith Polaroid filters rather than with red-greenglasses. This test is less dissociating than the origi-nal Worth four-dot test, where red and green in-duce retinal rivalry even in normals. Yet, the com-parison proposed by the authors of their test withthe Bagolini striated glasses test seems unwar-ranted. Contrary to the striated glasses test, thepolarized four-dot test does not present the patientwith a fusible stimulus in the fixation area. Hencethe higher percentage of central suppression de-tected with this test.

The reader should be aware that all informationderived from the current or past literature aboutthe presence, location, and depth of retinal sup-pression scotomas is tainted by our inability tocreate testing conditions that are identical to ca-sual conditions of seeing. Image separation with

red-green spectacles, polarizing filters, a screen-and-mirror arrangement, and even the phase dif-ference haploscope or Bagolini striated glassescreate conditions that are not entirely identical tothose in casual seeing. Numerous studies in recentyears have shown great variability, and contradic-tory results can be expected under different testingconditions.13, 38, 77, 93, 94, 137

Suppressing Versus Ignoring aDouble Image

The absence of spontaneous diplopia in a patientwith a manifest ocular deviation does not alwaysimply that suppression has developed. The patientmay have developed ARC (see p. 222). Otherpatients, especially older children and adults whoare no longer capable of developing suppression,simply learn to disregard the second image, espe-

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FIGURE 13–8. The Worth four-dot test. A, Lookingthrough a pair of red and green goggles, the patientviews a box with four lights (one red, two green, onewhite) at 6 m and at 33 cm (with the four lights mountedon a flashlight). The possible responses are given in B toE. B, Patient sees all four lights: peripheral fusion withorthophoria or esotropia with anomalous retinal corre-spondence. Depending on ocular dominance, the light inthe 6-o’clock position is seen as white or pink. C, Patientsees two vertically displaced red lights: suppression OS.D, Patient sees three green lights: suppression OD. E,Patient sees five lights. The red lights may appear to theright, as in this figure (uncrossed diplopia with esotropia),or to the left of the green lights (crossed diplopia withexotropia). (From Noorden GK von: Atlas of Strabismus,ed 4. St Louis, Mosby–Year Book, 1983.)

cially when the deviation is large and the secondimage appears in the periphery of the field ofvision. However, such patients easily can be madeaware of double vision by placing a light-red filterbefore one eye. The ability to ignore a disturbingsecond image is an entirely different process fromsuppression. The first occurs on a psychologicallevel, depends on the attention value of the imageto be ignored, and, as mentioned in the discussionof physiologic diplopia (see Chapter 2), is partof normal binocular vision. The second is activeintrinsic inhibition of afferent visual information.The distinction between suppression and ignoring

is of more than theoretical interest since the ab-sence of spontaneous diplopia may mislead theophthalmologist to assume that the strabismusproblem has been present since early childhood,when in fact the deviation may be of relativelyrecent onset, in which case a neuro-ophthalmo-logic evaluation may be required. Wright and co-workers163 found reduced pattern visual evokedpotentials (VEPs) in adults with acquired strabis-mus and absence of diplopia and concluded fromthese findings that cortical suppression had devel-oped in these patients. Unless it is also knownwhat, if any, effect the channeling of attentionfrom the images seen by one eye to those seen bythe other eye has on the VEPs, this conclusion isnot warranted.

Measurement of Depth ofSuppression

Suppression is not equally deep in all patients. Insome it may be readily overcome; in others it isdifficult to do so. It is useful and easy to establishhow deep the suppression is in a patient.

To make a patient aware of the images per-ceived by the deviated eye, one must reduce theretinal illuminance of the fixating eye until thepatient sees double. This is best done with a seriesof red filters of increasing density arranged in theform of a ladder (Fig. 13–9). Such a ladder mayconsist of gelatin filters, beginning with one layerand increasing to six or eight layers. The morelayers, the darker the filter. The patient fixates asmall light source, and the filters are placed infront of the fixating eye. Some patients see doublewith a single layer; others require three or morelayers before they recognize diplopia. The greaterthe number of layers needed, the deeper the sup-pression.5, 113

Laboratory experiments have produced datathat seem to contradict this common clinical find-ing. Holopigian’s data81 show that the depth ofsuppression is constant, regardless of changes incontrast, luminance, and spatial frequency of theinducing stimulus (see also Freeman and Jolly61).The reason for the difference between a commonand an easily observed clinical phenomenon andthese data is not at once obvious and may be dueto methodological variations.

Blind Spot Mechanism

Swan155 described a mechanism by which somepatients with 30� to 40� of esotropia make use of

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FIGURE 13–9. Red filter ladder.5 (Courtesy of Prof. BrunoBagolini, Rome.)

the blind spot to avoid diplopia. He later discov-ered the interesting fact that this possibility hadbeen mentioned by George Adams, optician to HisRoyal Highness, the Prince of Wales, in 1792.

The patients reported by Swan155 in his firstdescription of this mechanism had accommodativeesotropia with the following characteristics: (1)occasional diplopia and confusion of images, (2)esotropia of 12� to 18�, (3) blind spot of deviatingeye consistently overlying the fixation area, (4)good vision of each eye, (5) normal correspon-dence, and (6) good fusional potential demonstra-ble on haploscopic devices. In a later publication,however, Swan156 included a number of othergroups of patients who also utilized the blindspot mechanism. These were patients with sensoryabnormalities, amblyopia, anomalous correspon-dence, and suppression.

As pointed out by Olivier and von Noorden,123

many physiologic and clinical considerations indi-cate that the use of the blind spot to avoid diplopiais no more than a coincidence. The small size ofthe optic disk and the constant change of thedeviation with different fixation distances makes

the effectiveness of the use of the blind spot toelude diplopia improbable. Incessant slippage ofthe image from the blind spot to the adjacentretina would be unavoidable and cause intermit-tent diplopia with the need for continuous motorreadjustment to avoid double vision. We are notaware of such occurrences. Moreover, there is noknown physiologic mechanism, similar to a fixa-tion reflex, by which a retinal image would remainlocked onto the optic nerve head. Olivier and vonNoorden123 used the Bagolini glasses to examinepatients with characteristics of the blind spot syn-drome and found that the absence of diplopia inthe patient group described by Swan can be ex-plained by ARC. From these and other observa-tions, the conclusion was reached that the blindspot syndrome does not exist.123

Anomalous Correspondence

Basic Phenomenon and Mechanism

If one examines the visual field of a patient withheterotropia by placing a red filter in front of thehabitually fixating eye while the patient is lookingat a small light source, a number of differentresponses may be elicited (Fig. 13–10).

1. The patient may report that two lights areseen, a red one and a white one. In esotropiathe images appear in homonymous (un-crossed) diplopia, with the red light to theright of the white one when the red filter isin front of the right eye (Fig. 13–10A). Inexotropia the images appear in heterony-mous (crossed) diplopia, with the red lightto the left of the white light when the redfilter is in front of the right eye (Fig. 13–10B). If one now measures the distance be-tween the double images (e.g., on a Maddoxcross), one may find that this distance equalsthe amount of the previously determineddeviation. The response of this patient isnormal because it is the same as the re-sponse expected from a normally acting sen-sory system in the presence of a deviationof the visual axes. The patient has normalretinal correspondence (NRC). The patientmay report that only one pinkish light in theposition of the white fixation light is seen;that is, the red and white images appear tobe superimposed. This would be a normalresponse for someone whose eyes are

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FIGURE 13–10. Red filter test for sup-pression and anomalous retinal corre-spondence. NRC, normal retinal corre-spondence; ARC, anomalous retinalcorrespondence. For explanation, seetext. (From Noorden GK von: Atlas ofStrabismus, ed 4. St Louis, Mosby–YearBook, 1983.)

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straight. It is clearly an abnormal form oflocalization in the presence of a relativedeviation of the visual axes, and the follow-ing two possibilities exist.

2. The patient suppresses the image originatingfrom the deviated right eye (Fig. 13–10C).If under these circumstances a very dark-red filter is placed before the fixating eye,diplopia may still be elicited. The depth ofsuppression can be quantitated by increasingthe density of the filter held before the fixat-ing eye until the patient experiences diplo-pia.

3. The patient has ARC, that is, single binocu-lar vision occurs in the presence of a mani-fest strabismus. To distinguish between sup-pression and ARC a vertical prism is placedbase-up before the deviated right eye (Fig.13–10D and E). In the case of suppressionthe prism will move the white image abovethe suppression scotoma and the patient willexperience diplopia. The white image willbe localized correctly, that is, below and tothe right of the red image. When the whiteimage appears directly below the red imageit is localized incorrectly (Fig. 13–10E).This condition has been termed anomalouscorrespondence.

Consideration of the response in which thepatient perceived both images but localized themabnormally shows that normal coupling of the

FIGURE 13–11. Anomalous correspondence. A, The two hands are placed together so the fingersmatch, with the middle fingers representing the normal common foveal subjective visual direction.B, The fingers of the right hand are shifted so they no longer match, and two different foveal visualdirections are symbolized.

retinal elements of the two eyes is somehow bro-ken up and has been replaced by a new coupling.This concept is indeed the classic explanation ofthe observed phenomena. Anomalous correspon-dence is thought of as a shift of the subjectivevisual directions of the nonfixating eye relative tothose of the fixating eye, crudely symbolized inFigure 13–11.

Although anomalous correspondence is alwaysconsidered to be associated with strabismus orwith a history of such, it has been shown recentlythat it can occur or be induced in normal subjectsunder binocular stress.57 Binocular stress can beproduced by forced convergence, which is theintroduction of a change in the convergence stimu-lus without a coordinated change in the accommo-dative stimulus. A fixation disparity takes placethat causes a distortion of the nonius horopter (a‘‘dimple’’ is found). It is not clear at this timewhether these findings are of potential clinicalrelevance.

When one eye is constantly deviated, the ex-isting stimulus situation produces suppression sco-tomas in that eye. The normal relationship be-tween the two foveae is then loosened, and thevisual directions of the nonfixating eye shift. As aresult, the fovea of the fixating eye acquires ananomalous common visual direction with a periph-eral area of the nonfixating eye. This shift alsoimplies that the two foveae no longer have acommon visual direction. Anomalous correspon-

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dence therefore can be defined in two ways. Onemay say either that in this condition the two fo-veae have two different visual directions or thatthe fovea of the fixating eye has acquired ananomalous common visual direction with a periph-eral element in the deviated eye. Both these de-scriptions are important, since all tests for anoma-lous correspondence are based on one or the other.

Anomalous correspondence presumably adaptsthe sensory visual system to the abnormal motorcondition created by the deviation in an effort torestore some semblance of binocular cooperation.If the fovea of the fixating eye acquires a commonvisual direction with the area in the retina of thedeviated eye on which the fixation point is im-aged, the deviation is fully neutralized sensorially,that is, the shift in visual directions has fully offsetthe amount of the deviation. In this situation thesensory adaptation is most successful, and onespeaks of harmonious anomalous correspondencewhen both images in the red filter test coincide. Ifthe amount of the shift in visual directions doesnot fully compensate for the deviation, the adapta-tion is not complete and one speaks of unharmoni-ous anomalous correspondence.

Tests

All tests for determination of the status of thesensory relationship of the two retinas are neces-sarily subjective. Most clinicians have preferencesfor one or another test, and it is not necessary toperform all tests in each patient. However, it isnecessary to understand the principle underlyingthe most commonly used procedures. Basically alltests belong to one of two groups—diplopia-typeand haploscopic-type tests. The most commonlyperformed tests for retinal correspondence are theafterimage test, the Bagolini striated glasses test,and the determination of the angle of anomaly onthe major amblyoscope.

Afterimage Test

Hering75 found convincing proof for the unity ofthe binocular field in the following simple experi-ment. A small, lasting afterimage is produced inthe left eye, and the eye is then closed. In theopen right eye the afterimage appears in the fieldof vision and shifts with the movements of theeyes, just as if the left eye were open. Afterimagesproduced successively on the foveae of the twoeyes will appear in their common visual direction,

regardless of whether the eyes are open or closedand regardless of the position of the eyes relativeto each other. Afterimages therefore appear to bean ideal means of studying the sensory relation-ships of the retinas. Bielschowsky19 applied thistest on a large scale to the examination of patients,and the afterimage test has become one of themost widely used tests for retinal correspondence.

In clinical practice the test is performed byusing a battery-powered camera flash (Fig. 13–12)to produce a vertical afterimage in one eye and ahorizontal afterimage in the other eye. The re-flecting surface is covered with black paper toexpose a narrow slit, the center of which is cov-ered with tape and serves as a fixation mark, thusprotecting the fovea from exposure. The resultingafterimage is that of a line with a break in itsmiddle, which represents the fovea. The patient isrequired to fixate steadily the central mark, firstwith one eye while the slit is in a horizontalposition (Fig. 13–13A), and then with the othereye while the slit is in a vertical position (Fig.13–13B). The nonexposed eye must be well cov-ered. During the exposure, a strong stimulusreaches the principal horizontal and vertical me-ridians of the right and left eyes but in neither eyeis the foveal area stimulated. In a darkened roomor with the eyes closed, the patient now sees thetwo successively imprinted afterimages simultane-ously as positive afterimages (bright lines). Ina lighted room or with the eyes open, negativeafterimages (dark lines) will be seen. The regionof the fovea will appear as a gap in each line.

FIGURE 13–12. Camera flash attachment for afterim-age test.

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FIGURE 13–13. Afterimage test. For expla-nation, see text.

These gaps will be seen in the same direction, thatis, superimposed, if the foveae have the samevisual direction. Consequently, the two afterim-ages will be seen in the form of a cross with asingle hole in the center (Fig. 13–14A), whichindicates that correspondence is normal.

If the vertical afterimage with its central holeappears to the left or to the right of the hole inthe horizontal afterimage, this displacement im-plies that the two foveae have different visualdirections, that is, there is anomalous correspon-dence (Fig. 13–14B and C).

The test can be performed in normally devel-oped children as young as 4 years of age. Duringthe exposure, the examiner must observe patientsclosely and those with wandering or eccentricfixation (see Chapter 14) must be excluded fromthe test. This is because the localization of theafterimage created in an eccentrically fixating eyeno longer corresponds to the principal visual direc-tion but to a secondary one. If the test is applied

to such patients for special purposes, the positionof the stimulating light on the retina of the devi-ated eye relative to the fovea must be taken intoaccount in evaluating the test result. For instance,if there is identity between the angle of anomalyand the degree of eccentricity, localization of theafterimages in the form of a cross may then indi-cate NRC rather than ARC! Suppression of thepoorer eye or alternating fixation at times mayinterfere greatly with visualization of both afterim-ages. To minimize these difficulties, it is advisableto use certain precautions. The fixating eye shouldalways be exposed first to the flash placed in ahorizontal position. The habitually deviated eye isthen exposed to the vertical flash. Always produc-ing the vertical afterimage in the habitually devi-ated eye will ensure uniform data that show at aglance the state of the retinal correspondence.

Of greatest importance for understanding theafterimage test is the realization that once theafterimages have been imprinted, their relation

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FIGURE 13–14. Afterimage test. A, Normal localization (cross) in normal correspondence (NRC). B,Anomalous crossed localization (ARC) in a case of esotropia. C, Anomalous uncrossed localization ina case of exotropia.

remains unchanged, regardless of any laterchanges in the position of the eyes. This is onegreat advantage the afterimage test has over allother tests for retinal correspondence. In othertests, changes in the position of the eyes willcause a shift of the images on the retina andtherefore a change in the stimulus situation. Nochange in the stimulus situation can occur as aresult of eye movements once the afterimageshave been produced. This point cannot be empha-sized strongly enough. To prove it, the reader needonly produce an afterimage in each eye and thenmove the eyes in any direction of gaze, convergevoluntarily, or gently push one eye with a fingerto one side. No change in the relative position ofthe afterimages will take place.

In some clinical situations it may appear as ifa change in the position of the eyes had indeedcaused a change in the relative position of theafterimages. For example, a patient with intermit-tent exotropia may report that afterimages in theform of a cross are seen when the eyes are alignedbut that they are separated when the patient allowsone eye to deviate. This phenomenon can be ob-served frequently in patients with this conditionand has been used to support the notion that extra-retinal signals from proprioception sensors in theextraocular muscle influence the relative positionof the afterimages.129 However, this change is not

a result of the movement or the divergent positionof the eyes but of a change from normal to anoma-lous correspondence.158

Striated Glasses Test of Bagolini

All tests for retinal correspondence introduce anartificial situation that may affect the test result toa greater or lesser degree. To minimize the influ-ence of the testing procedure, Bagolini6 devised atest that permits an evaluation of the sensory reti-nal relationship under conditions that come asclose as possible to natural conditions of seeing.

The striated glasses are plano glasses withoutrefractive power that do not modify the state ofaccommodation. They have fine parallel linearstriations that do not alter significantly the visualacuity and the perception of the visual space. Thepatient fixates a small light, at the reading distanceor at the end of the examination lane, through thestriated glasses placed before each eye in a trialframe. The glasses are usually placed at 45� and135�. Optical correction should be worn duringthe test. Through each striated glass the fixationlight is perceived as crossed by an elongatedstreak across one meridian. The light source is afusible stimulus, equal for each eye. The striationsare check marks and allow differentiation of asingle perception of the light due to suppression

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(one streak) from binocular perception in normalsor patients with ARC (two streaks crossed in thecenter) or from diplopia (two streaks separatefrom each other or crossing in the peripheral partof the streaks).

Figure 13–15 shows the appearance of thestreaks as they may be seen by a patient and theinterpretation of this test.

The striated glasses may also be used in con-junction with the red filter bar of Bagolini (seeFig. 13–9), for evaluating the strength of the nor-mal binocularity or of the binocular sensorial ad-aptation.12 In this way it is possible to establish theamount of dissociation necessary for disrupting

FIGURE 13–15. Use of striated glasses to test for suppression and anomalous retinal correspon-dence (ARC). A, Crossing of the luminous lines when a manifest ocular deviation (cover test) ispresent indicates ARC. B, Suppression of the right eye. C, Fixation point scotoma (with manifestdeviation and ARC) or foveal scotoma (with orthophoria and normal retinal correspondence) of theright eye. D, Double vision with esotropia.

binocular cooperation (normal or anomalous) andto know which image belongs to which eye.

The usefulness of the Bagolini striated glassesfor measuring cyclotropia under nearly normalconditions of seeing is discussed in Chapter 12and yet another application for their use duringmonocular and binocular investigation of the vi-sual field has been recently proposed.80

Testing With the Major Amblyoscope

This test is illustrated in Figure 13–16. Both armsof the instrument area are moved by the examinerwhile alternately flashing the light behind each

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FIGURE 13–16. A–C, Testing with the major amblyoscope for retinal correspondence. NRC, Normalretinal correspondence; UHARC, unharmonious retinal correspondence. For explanation, see text.(From Noorden GK von: Atlas of Strabismus, ed 4. St Louis, Mosby–Year Book, 1983.)

slide until there is no further fixation movementof the patient’s eye. The angle of strabismus (20Din Fig. 13–16A) determined in this manner iscalled the objective angle. The arms of the majoramblyoscope are now placed so that the targetsare imaged on the two foveae of the patient’s eyes.If normal correspondence exists, the images oftwo dissimilar targets appear to be superimposed.In the presence of anomalous correspondence andif the patient is esotropic, there will be crosseddiplopia; if the patient is exotropic, uncrosseddiplopia will occur.

To determine the degree of shift in visual direc-tions (the so-called angle of anomaly), proceed inthe following manner: Both arms of the instrumentare moved by the examiner while alternatelyflashing the light behind each slide until there isno further fixation movement of the patient’s eye(alternate cover test; Fig. 13–16A). Each arm ofthe instrument is now set at 10� ET (esotropia);this patient has an ET of 20�. The angle of strabis-mus determined in this manner is called the objec-tive angle. If the patient sees the visual targetssuperimposed when the instrument is in this posi-

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tion, his subjective angle equals the objectiveangle; NRC is present. When the patient reportsthat the targets are separated with the instrumentset at the objective angle, ARC is present. Thepatient’s foveae no longer have a common visualdirection (paradoxical diplopia, p. 237). When thepatient reports superimposition of the visual tar-gets with the instrument arms set at zero (Fig.13–16B), the subjective angle is zero and retinalcorrespondence is abnormal. In this case, theangle of anomaly equals the objective angle andthe sensory adaptation is complete; anomalouscorrespondence is said to be harmonious. Whenthe angle of anomaly is smaller than the objectiveangle (Fig. 13–16C ), unharmonious retinal corre-spondence is present. In this drawing, a patientwith 20� ET reports superimposition with the armsof the instrument set at 10� ET. The sensory adap-tation is incomplete; the subjective angle issmaller (10� ET) than the objective angle (20�

ET) but larger than zero. In most instances, unhar-monious retinal correspondence can be explainedon the basis of a secondary enlargement of theobjective angle. Some authors have suspected thatthis finding is an instrument artifact.22, 25

The determination of retinal correspondencewith a major amblyoscope may be difficult be-cause of suppression and changes in the mode oflocalization. Experience and skill in overcomingthese difficulties and the ability to interpret patientresponses correctly are required to obtain usefulinformation by this method. The following testsmust be considered ancillary but may be usefulunder special conditions and for research pur-poses.

Diplopia Test

The diplopia test with a red filter, shown in Figure13–10, requires excellent patient cooperation. Thepatient’s deviation is first determined objectively,and the diplopia test is then performed at the samefixation distance and with the same refractive cor-rection to permit comparison. The test can bequantitated when a tangent scale or screen is avail-able by asking the patient where the red light isseen in relationship to the fixation light.

The red filter test may also be performed afterreducing the deviation fully by prisms. When thisis done, the two foveae are simultaneously stimu-lated by the fixation light. With simultaneous stim-ulation of the two foveae, patients with anomalouscorrespondence may suddenly revert to normal

correspondence and see double.30, 32 The red filtertest is time-consuming and therefore rarely per-formed in clinical practice.

Testing With Projection Devices

Projection methods (Lancaster red-green test, Po-laroid projection method of Burian, and the phasedifference haploscope of Aulhorn) (see Chapter 4)do not differ in principle from the major amblyo-scope. They also use two targets that are presentedseparately in haploscopic fashion to the two eyes.However, these methods are generally more flex-ible and avoid proximal convergence since theyare used in distance fixation.

Targets used in these devices may be placed invarious positions on the screen, either superim-posed or displaced at the objective angle of thepatient or in any other desired position. Thus anydesired stimulus situation may be achieved. Insearching for the subjective angle, the patient mayhandle one of the projectors.

Foveo-Foveal Test of Cuppers

As stated earlier, it is not possible to do theafterimage test unless the patient fixates reason-ably well with the foveal area. To overcome thisdifficulty, Cuppers50 devised a test that permitsinvestigation of the foveo-foveal relationship inpatients with eccentric fixation. An asterisk isplaced on the fovea of the deviated eye underophthalmoscopic guidance while the other eyefixates the light on a Maddox cross or tangentscreen (Fig. 13–17A). If one can break through thesuppression scotoma of the deviated eye, which isgenerally possible, the patient can then report tothe examiner the position of the images. If thefixation target appears to be superimposed on thecentral fixation light of the Maddox cross thefoveae have a common visual direction, that is,retinal correspondence is normal (Fig. 13–17B).In the presence of anomalous correspondence thefoveae have different visual directions and theasterisk will be superimposed on one of the num-bers on the horizontal bar of the Maddox scale.This number indicates the angle of anomaly indegrees (4� in Fig. 13–17C).

This procedure has great intrinsic accuracy, butone must keep in mind that simultaneous stimula-tion of the two foveae may result in changesof localization. Similar reasoning applies to theafterimage test. In the latter, however, pure foveal

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FIGURE 13–17. The foveo-foveolar test of Cuppers.51 A,Schematic representation of the testing arrangement. Ifthe test is performed at 5 m distance from the Maddoxscale the larger figures indicate the angle of anomaly.The small figures (not shown) are valid for a testingdistance of 1 m. This patient has eccentric fixation OD;e indicates the fixation area. B, Patient sees the asterisksuperimposed on the central fixation light of the Maddoxscale. The two foveae have a common visual direction(NRC, normal retinal correspondence). C, The asteriskappears over the number 4 on the horizontal bar of theMaddox scale. The two foveae have acquired differentvisual directions (ARC, anomalous retinal correspon-dence). The angle of anomaly in this case is 4�. (FromNoorden GK von: Atlas of Strabismus, ed 4. St Louis,Mosby–Year Book, 1983.)

stimulation is avoided. A modification of the fo-veo-foveal test consists of producing a verticalafterimage on the principal vertical meridian ofthe fixating eye and stimulating the foveal area ofthe deviated eye by means of Haidinger’s brushes.

Evaluation of Tests

If anomalous correspondence represents an adap-tation to the prevailing conditions in which a pa-tient uses his or her eyes, tests that duplicate theseconditions should provide ready evidence of thisadaptation. Tests that are foreign to the visual

experience of the patient should be least likely todo so. One should expect anomalous correspon-dence, especially the harmonious type, to occurmore frequently with the first type of test thanwith the second type. The diplopia test and themajor amblyoscope test are close to the naturalconditions of seeing,30 and the afterimage test isthe farthest removed. However, the striated glassestest of Bagolini6 fulfills best the requirement ofinterfering minimally with the patient’s use of hisor her eyes. Partly for this reason and partly be-cause of its convenience and extreme ease ofexecution, this test is the test most widely andsuccessfully applied in clinical practice.

Bagolini and Tittarelli14 found harmoniousanomalous correspondence in 83% of their pa-tients, using the striated glasses, but in only 13%,using the synoptophore. With the synoptophore53% of the patients were found to have an unhar-monious anomalous response. Conversely, normalcorrespondence was noted in only 10% tested withthe striated glasses test, but when the synopto-phore was used this figure was 40% (Table 13–1).Pasino and Maraini125 made similar observations,but the percentage of patients with harmoniousanomalous correspondence tested with the striatedglasses test was considerably lower.

There was a great discrepancy between thenormal responses from the afterimage test (51%)and a major amblyoscope (7%) in the 100 patientsreported on by Burian and Luke.35 They foundanomalous correspondence in 30% with the stri-ated glasses test, in 84% with the major amblyo-scope, and in only 27% of patients with theafterimage test (Table 13–2). Generally speaking,all these data confirm the hypothesis that in alarger number of patients there tends to be ananomalous response in tests that interfere leastwith the ordinary conditions of seeing. The ratherwide numerical differences in the various reportedseries no doubt reflect the heterogeneity of thematerial. Esotropes and exotropes respond differ-ently, as do the various subgroups among thesepatients. Only a detailed analysis of the cases andunified classification will reconcile these differ-ences.

The emphasis placed on the data obtained withtests that closely imitate natural conditions ofseeing carries the implication that other tests giveresults that are unreliable or are of no clinicalsignificance. This conclusion is not justified. It isclearly of interest to know how a patient’s eyesare used in daily life, especially if one wishes to

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TABLE 13–1. Comparison of Results of Determination of Status of Sensory Response ofStrabismic Patients Using Various Methods of Testing

Normal AnomalousCorrespondence Correspondence Suppression Diplopia

Striated glasses 3.8% 83.4% (harmonious) 9.7% 2.9%Worth four-dot test 0% 33.9% (harmonious) 56.3% 9.7%Major amblyoscope 34.9% 12.6% (harmonious) 0% 0%

(synoptophore) 52.4% (unharmonious)

Modified from Bagolini B, Tittarelli R: Considerazioni sul meccanismo antidiplopico nello strabismo concomitante. Boll Ocul 39:211, 1960.

assess spontaneous changes, as after operations,or changes induced by other therapeutic measures;but for the evaluation of the patient’s total condi-tion, especially from a prognostic standpoint, it isjust as significant to know that normal correspon-dence can be elicited with some of the tests as itis to know that there is harmonious anomalouscorrespondence in ordinary environmental situa-tions. One is reminded of Chavasse’s dictum ex-pressed in his inimitably vivid prose: ‘‘The opti-mist, at all events, will agree that, with therestoration of normal function in view, it is moreimportant in any given case to seek out the rem-nant of normal sensory correspondence than mor-bidly to uncover the nakedness of the abnor-mal.’’45, p. 455

Why do certain tests produce normal responsesand others anomalous responses? As has beenpointed out repeatedly, in the development ofanomalous correspondence the innate normal sen-sory relationship is only gradually replaced and

TABLE 13–2. Comparison of Determination of Sensory Response in 100 Patients withHeterotropia Using Three Different Methods

Mixed ARC ARC/ UnreliableNRC ARC and NRC Suppression Suppression Response Total

All 100 patientsStriated lenses 11 30 5 24 24 6 100Major amblyoscope 7 84 0 0 8 1 100Afterimage test 51 27 7 2 9 4 100

All 80 esotropic patientsStriated lenses 6 27 2 23 18 4 80Major amblyoscope 6 65 0 1 8 1 80Afterimage test 42 21 5 2 6 4 80

All 20 exotropic patientsStriated lenses 5 3 3 1 6 2 20Major amblyoscope 1 19 0 0 0 0 20Afterimage test 9 6 2 0 3 0 20

NRC, normal retinal correspondence; ARC, anomalous retinal correspondence.Adapted from Burian HM, Luke N: Sensory retinal relationships in 100 consecutive cases of heterotropia. A comparative clinical study.

Arch Ophthalmol 84:16, 1970.

then not always completely. Patients who readilyadapt their sensory systems to changes in thestimulus situation—and these seem to represent amajority—may have a superficial rearrangementof their sensory system. In those patients with along-standing deviation or in those with an abilityto adapt more completely, anomalous correspon-dence is more deeply rooted, and normal re-sponses may be elicited only with difficulty, if atall. In those in whom a deviation is not of longstanding, anomalous correspondence can be elic-ited only if the tests closely duplicate the ordinaryenvironmental conditions.

Tests currently in use to diagnose ARC arelisted in Figure 13–18 in ascending order ac-cording to their dissociating power. The chart ismodified from Bagolini,8 who defined dissociationas the property of a test to alter the casual condi-tions of seeing.76, 134 For practical purposes andto assess correspondence under the least and mostdissociating conditions, we advocate use of the

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Examination of the Patient—III 233

FIGURE 13–18. Tests for retinal corre-spondence listed in order of their disso-ciating effect. (Modified from BagoliniB: I. Sensorial anomalies in strabismus(suppression, anomalous correspon-dence amblyopia). Doc Ophthalmol41:1, 1976.)

Bagolini glasses and of the afterimage test. An-other option is to use the striated glasses in con-junction with the Bagolini red filter bar.

Neurophysiologic Basis

The neurophysiologic basis of ARC is beginningto unravel. Animal experiments, which thus farhave only been performed in eso- and exotropiccats, have shown strabismus-induced modificationof the lateral suprasylvian cortex. Receptive fieldsof binocularly driven neurons were found to belocated on noncorresponding retinal points.52,

64, 148 It is necessary to repeat these experiments inprimates to further explore the possibility that thisadaptive shift of spatial coordinates could formthe neural basis for ARC.

Dengler and Kommerell54 addressed the ques-tion of whether anomalous correspondence occursbetween disparate retinal elements that have ac-quired new interocular connections or whether theexisting connections in normal humans suffice tosubserve anomalous correspondence. Theyshowed in normal subjects that interocular connec-tions reach over disparities as large as 21�. Thisheld true not only for connections between sym-metrical areas in the retinal periphery of both eyes(bitemporal and binasal) but also for connectionsbetween the fovea of one eye and the temporalperiphery of the other eye. Crossed disparitiesreach over wider angles than nasal disparities.These findings suggest the possibility that ARCoccurs on the basis of connections that alreadyexist in normal subjects and that the anatomical

basis for large angle anomalous correspondencecould be better for exotropes than for esotropes.

Suppression and AnomalousCorrespondence

Suppression and anomalous correspondence docoexist in patients with comitant strabismus, a factthat has been known since the early studies ofTschermak-Seysenegg158 and Bielschowsky.18

Travers,157 who made a thorough investigation ofthe relation of suppression scotomas, amblyopia,and anomalous correspondence, believed that sup-pression was a prerequisite of establishment ofanomalous correspondence. Harms70 went so faras to say that proving the presence of regionalsuppression scotomas was equivalent to demon-strating that there was anomalous correspondence.Hallden68 showed that suppression scotomas doexist in the fovea and that part of the peripheralretina of the deviated eye receiving the same im-age as the fovea (fixation point scotoma). Herzau77

reported similar findings.In esotropes fixation point scotomas are small

and well circumscribed, but occasionally theyreach hemianopic proportions in exotropes withanomalous correspondence.68 Suppression scoto-mas are found not only in the deviated eye butalso at the point in the peripheral retina of thefixating eye at which the same image is receivedas that on the fovea of the deviated eye.71, 77 Ac-cording to Herzau,78 harmonious anomalous corre-spondence may permit anomalous binocular visiononly between those parts of the two retinas in

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which nonsignificant functional differences existbetween retinal elements that receive identical im-ages. In other areas of the binocular visual field,anomalous correspondence permits optimal per-ception of visual detail by suppressing the moreperipherally located retinal points.

Campos38 challenged this view and pointed outthat most studies in which suppression scotomaswere detected in patients with anomalous corre-spondence were performed with perimetric tech-niques that caused dissociation of the eyes orretinal rivalry. He used fusible test targets andnondissociating perimetric techniques and controlmarks and demonstrated that areas of single per-ception, interpreted by others as being caused bya suppression scotoma, are actually areas of binoc-ular perception.109 Campos36 proposed that in somestrabismic patients, particularly in those with asmall angle deviation, ARC functions as the onlyantidiplopic mechanism and that even amblyopiamay develop in such patients without suppressionand from an ‘‘inhibition of normal directional lo-calization.’’ This means that reduced visual acuityof the amblyopic eye cannot be explained exclu-sively with prolonged suppression of its fovea.The inhibition of normal directional localizationmay be considered as an additional amblyopio-genic factor. This should not distract from the factthat the central portion of the streak, produced bya Bagolini glass before the deviated eye, is miss-ing in most patients with small angle esotropia(see Fig. 13–15C). There is no interpretation otherthan that of a fixation point scotoma for this phe-nomenon.

The view that suppression and anomalous cor-respondence exclude each other to a degree isalso supported by Bagolini and Tittarelli14 andBagolini.10 Using the striated glasses test, theyfound that harmonious anomalous correspondenceis present in patients with low degrees of strabis-mus of 30� or less, whereas suppression is therule in patients with larger deviations. Others haveconfirmed these findings.37, 87, 125

The enormous variations regarding the relation-ship between the deviation size, type of strabis-mus, and prevalence of ARC reported in the olderliterature can only be explained by differences intesting procedures and the heterogeneity of thepopulations under study.

Development and Clinical Picture

Normal correspondence is a stable innate condi-tion that cannot be altered experimentally in hu-

mans, but this stability is not so rigid as not toallow for changes if abnormal conditions warrantthem. When a disturbance in the motor conditionsis present, such as a deviation of the visual axesin comitant strabismus, a profound rearrangementin the sensory system takes place, which is ex-pressed in the sensory symptoms of strabismus.

Adaptability is a general characteristic of thevisual system. It reacts with appropriate responsesto changes in the environment, that is, the stimulusconditions. Accommodation, dark adaptation, Pa-num’s area of single binocular vision, and anoma-lous correspondence are obvious examples. Allthese functions are useful, but the teleologicalmeaning of the term adaptation must not be exag-gerated. Anomalous correspondence is the resultof a physiologic mechanism that takes place re-gardless of its usefulness to the organism. It is nota ‘‘psychological’’ interpretive phenomenon.

Development

Whatever the mechanism of anomalous correspon-dence, a study of a large number of patients withcomitant heterotropia has shown that certain fac-tors are necessary for its establishment.30 First, acertain flexibility of the sensory visual system isrequired. This flexibility decreases with the pass-ing of years. Anomalous correspondence thereforeis found in patients in whom the deviation of thevisual axes arose early in life, as stressed by vonGraefe.63 Adults who acquire such a deviationmaintain normal correspondence, but abnormalcorrespondence may be found in patients with adeviation of early onset when they are examinedlater in life. There are various reasons for suchbehavior.

To break through the innate retinocortical rela-tionship requires time. The stimulus situation thatleads to establishment of anomalous correspon-dence must persist for a sufficiently long periodto produce its result. Consequently, the more con-stant the magnitude of the deviation and the moreconstantly a patient uses the same eye for fixation,the more readily anomalous correspondence willbe established. Instability of the deviation andfrequent changes in fixation tend toward mainte-nance of the normal retinocortical relationship.Normal correspondence is not immediately andrarely totally suppressed. Normal and anomalouscorrespondence frequently coexist in the same pa-tient, especially in those with intermittent exotro-pia. The Hugonniers have introduced the term

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Examination of the Patient—III 235

duality of correspondence for this phenomenon.83

Others have shown that different patterns of reti-nal correspondence may affect the central andperipheral visual fields.149, 150 Retinal correspon-dence tended to be closer to normal in the centralparts and anomalous in the more peripheral partsof the visual field.

It has been shown that in development ofanomalous correspondence the angle of anomalygradually increases until it equals the amount ofthe deviation and the anomalous correspondencebecomes harmonious.67, 68 A gradual decrease inthe angle of anomaly has also been reported dur-ing the process of normalization by treatment.44

This gradual increase and decrease may well betrue during the periods of establishment and re-gression of anomalous correspondence. However,once established, a reversal from anomalous tonormal correspondence and vice versa may occurwithin seconds or fractions of a second.

The sensitive period during which anomalouscorrespondence develops is not exactly known be-cause the precise onset of strabismus and its con-stancy are difficult to assess in young children byhistory alone. It is our clinical impression, how-ever, that the capacity to develop ARC, even ifonly superficially seated, extends beyond the sen-sitive period established for amblyopia (Chapter14) and into the early teens.

Clinical Picture

For all the reasons stated above, responses ofpatients to the different tests for anomalous corre-spondence, and indeed to the same test, may bevaried and are often described as confusing oreven frustrating to the examiner. Jampolsky89 isquoted as having remarked that ‘‘the world wouldbe a happier place if no one had thought aboutanomalous retinal correspondence.’’ However, ifthe basis of each test and the processes involvedare clearly understood, the patient’s responses be-come meaningful and provide indispensable infor-mation about the degree of normal or anomalousbinocular cooperation.

As has been pointed out, anomalous correspon-dence is not established with equal firmness in allpatients. It is necessary to list and describe someof the more common variants that make up theclinical picture of anomalous correspondence.

HARMONIOUS ANOMALOUS CORRESPON-

DENCE. This mode of localization has already

been described and should not be difficult to un-derstand. The patient in Figure 13–19 demon-strates that the angle of anomaly equals the devia-tion. The motor and sensory conditions are ingood accord.

UNHARMONIOUS ANOMALOUS CORRESPON-

DENCE. If the angle of anomaly is smaller thanthe angle of squint, adaptation to the deviation isincomplete. The explanation for this situationposes questions that have been answered in vari-ous ways. It has been suggested that it is anartifact of some testing situations.67, 102 This isquite possible; however, other investigations haveshown that this is not always the case and thatunharmonious anomalous correspondence is agenuine clinical entity.4, 31, 78 To explain this puz-zling phenomenon, Rønne and Rindziunski136 sug-gested that in some patients the gradual increaseof the angle of anomaly, postulated by Travers,157

stops before reaching the stage of harmoniousanomalous correspondence. Burian30 emphasizedand cited many examples in which a more or lesssudden change in the angle of squint preceded thefinding of an unharmonious anomalous localiza-tion. The cause for this change may be known(prescription of glasses, prismatic corrections, oroperations) or unknown.

PARADOXICAL DIPLOPIA. The obvious exampleof an unharmonious anomalous correspondence isparadoxical diplopia. It occurs when anomalouscorrespondence persists after surgery, and the

FIGURE 13–19. Superimposition with harmonious anom-alous retinal correspondence. (From Burian HM: Adaptivemechanisms. Trans Am Acad Ophthalmol Otolaryngol57:131, 1953.)

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236 Introduction to Neuromuscular Anomalies of the Eyes

postoperative position of the eyes no longer con-forms to the preoperatively established angle ofanomaly. Esotropic patients whose eyes have beenset straight, or almost straight, may exhibit in oneor all tests a crossed localization of the fovealor parafoveal stimuli31 (Fig. 13–20), and formerexotropic patients whose eyes have been surgi-cally aligned will experience uncrossed diplopia.Clearly, disharmony between the motor and sen-sory conditions is present, and these patients re-spond with a type of diplopia that is contraryto what one would expect on the basis of thepostoperative position of the eyes.

Paradoxical diplopia can nearly always be elic-ited in patients with anomalous correspondencewhen both foveae are stimulated simultaneouslywith the major amblyoscope or when the positionof the afterimages during the afterimage test iscompared with the underlying deviation. For ex-ample, an esotrope with anomalous correspon-dence will localize a horizontal afterimage pro-duced in the right eye to the left (crossed) of avertical afterimage produced in the left eye (seeFig. 13–14B).

In deep-rooted harmonious anomalous corre-spondence, the amount of the postoperativecrossed diplopia may be used to guess at theamount of the preoperative deviation. For exam-ple, if a patient has 5� of residual esotropia and ifthe angle of anomaly determined postoperativelyequals 25�, the patient in all probability originallyhad a deviation of 30�.

From a clinical point of view, paradoxical di-

FIGURE 13–20. Crossed (paradoxical) diplopia aftersurgical alignment in a formerly esotropic patientwith persistent anomalous correspondence. (FromBurian HM: Adaptive mechanisms. Trans Am AcadOphthalmol Otolaryngol 57:131, 1953.)

plopia is a fleeting phenomenon limited to theimmediate postoperative period. Rarely does itpersist longer than a few days or weeks; however,there are exceptions. We have examined a patientin whom paradoxical diplopia persisted for 2 yearsafter surgery.

CASE 13–1

This 38-year-old man had had exotropia since child-hood. He had undergone muscle surgery on theright eye for a deviation of 35� before we saw him.The patient had experienced double vision since theoperation. The prism cover test revealed a residualexotropia of 10� at near and distance fixation. Thepatient had uncrossed diplopia. The afterimage testand the Bagolini striated glasses test revealed ARC.Diplopia disappeared with a 25� base-out prism.

The sensory state of the patient in Case 13–1is shown in Figure 13–21. The image in the righteye falls nasal to a retinal area that still shares acommon visual direction with the fovea of the lefteye and therefore it is localized to the right of thepatient in an uncrossed fashion. The preoperativedeviation of 35� exotropia corresponds with thepersisting angle of anomaly since a 25� base-outprism is required to eliminate the image. This casedemonstrates the practical importance of analyz-ing with the red-glass test postoperative diplopiato determine whether it is paradoxical or in accor-dance with a residual deviation.

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Examination of the Patient—III 237

FIGURE 13–21. Paradoxical diplopia in exotropia. ARC,anomalous retinal correspondence. See text for explana-tion.

CHANGES IN LOCALIZATION WITH CHANGE IN

FIXATION. The sensory system of a patient whofixates habitually with one eye is adjusted to thismotor condition. If forced in a test situation toassume fixation with the other eye, the patientmay continue to localize anomalously; or quitefrequently if the anomalous correspondence is notfirmly established, the patient will revert to normalcorrespondence. Such behavior is a good prognos-tic sign. It was made use of in orthoptic techniquesfor treatment of anomalous correspondence (Wal-raven technique162).

MONOCULAR DIPLOPIA (BINOCULAR TRI-

PLOPIA). In so-called paradoxical diplopia, anom-alous localization is maintained after operativealignment of the eyes. Under the same circum-stances, another phenomenon, known as monocu-lar diplopia or binocular triplopia, may be ob-served. The patient perceives two images of thefixation object with the deviated or formerly devi-

ated eye, one localized normally and the otheranomalously. In binocular viewing the patient willthen perceive three images, one with the fixatingeye and two with the deviated eye, one to eachside of the image seen by the fixating eye (Fig.13–22). Thus if there is a residual right esotropiaof, say, 4� or 5�, the patient will have an uncrosseddiplopia in that amount relative to the object seenby the fixating left eye and, at the same time, acrossed diplopia equal in amount to the preopera-tive angle of anomaly (minus the amount of un-crossed diplopia). Characteristically, the un-crossed, normally localized image is at first thedimmer of the two (see Fig. 13–22). As time goeson, the crossed image gradually fades and mayeventually disappear, while the uncrossed imagestrengthens as the normal correspondence be-comes reestablished.

BINOCULAR TRIPLOPIA. First mentioned by Ja-val90 binocular triplopia was observed in the formof monocular diplopia in the now famous caseof the ‘‘moderately well-educated and intelligentelectrician Georg Sturm’’ reported in 1898 byBielschowsky.17 This patient had a long-standingstrabismic amblyopia and lost his good eyethrough a perforating injury. Shortly after the in-jury he began seeing double with his amblyopiceye. The meticulous analysis and interpretation ofthis patient’s problem launched Bielschowsky onhis career as one of the foremost experts in strabis-mus of his time. He explained the phenomenoncorrectly on the basis of a competition betweennormal and anomalous relative localization: thefovea of the amblyopic eye localized one visualobject simultaneously in two visual directions, theinnate normal and the acquired anomalous one.Monocular diplopia has since been much misinter-preted.34 The inadequate attempts at other explana-tions only confuse the uninitiated who try to un-derstand the phenomenon. In rare cases binoculartriplopia occurs spontaneously, but just like para-doxical diplopia, binocular triplopia can frequentlybe provoked instrumentally. Cass44 was able toproduce it with the synoptophore in 30 out of 70patients by appropriate stimulation, and Walra-ven162 used it to develop a special orthoptic tech-nique for treatment of anomalous correspondence.

POSTOPERATIVE CHANGES IN CORRESPON-

DENCE AND INSTANTANEOUS CHANGES IN

THE ANGLE OF ANOMALY. Bielschowsky20 andOhm122 followed spontaneous changes in the sen-

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238 Introduction to Neuromuscular Anomalies of the Eyes

FIGURE 13–22. Appearance of fixated object seenin binocular triplopia. (From Burian HM: Adaptivemechanisms. Trans Am Acad Ophthalmol Otolaryn-gol 57:131, 1953.)

sory relationship of the eyes after operations forstrabismus. Ohm postulated three stages in thisdevelopment. In the first stage, correspondenceremained anomalous; in the second, rivalry oc-curred between normal and anomalous correspon-dence; and in the third, normal correspondencewas reestablished in favorable cases. Ohm recog-nized that not every patient goes through all threestages and that development may stop at anystage. He believed that the patient’s age at thetime of the operation, individual adaptability, thedepth with which anomalous correspondence wasestablished preoperatively, and the use the patientmade of the eyes influenced this development.122

These descriptions of the postoperative devel-opment of anomalous correspondence in olderpublications agree with the concept emphasizedpreviously, that development of anomalous corre-spondence requires time. However, Hallden67 wasable to demonstrate an instantaneous change inthe angle of anomaly in patients with esotropiaand harmonious anomalous correspondence. Hall-den likened these covariations to the fusionalmovements of subjects with normal binocular vi-sion. Rønne and Rindziunski135 claimed that theycould even induce changes in the position ofafterimages by quickly moving a prism rack infront of one eye. This startling finding was par-tially confirmed by Hansen and Swanljung.69

More recently Bagolini,7 among others, foundthat there is an immediate postoperative adaptationto the newly created deviation, so that a harmoni-ous anomalous correspondence can be measuredas soon as the patient can be tested. This interest-ing finding, which we have been able to confirm,

must not be misinterpreted to indicate that a newsystem of ARC develops within days after surgery.Rather, it appears that there are an infinite numberof retinal elements between the fovea and thepreoperative fixation point that are capable ofsharing a common visual direction with the foveaof the fixating eye (point-to-area relationship). Re-duction of the angle of strabismus by surgerymerely shifts the retinal image in the deviatingeye closer to the fovea but within an area that hadcorresponded preoperatively with the fovea of thesound eye. This point-to-area vs. point-to-pointconcept of ARC is useful also in explaining adap-tation of the angle of anomaly to variations of theangle of squint at different fixation distances. Thisconcept is supported further by the observationthat anomalous correspondence may be present inprimary position, as well as in upgaze or down-gaze in patients with A and V patterns of strabis-mus.46, 74

Thus the angle of anomaly may adapt to con-siderable variations in the angle of strabismus.Even though these and other clinical findings4

indicate that there may be numerous peripheralretinal points in the deviated eye capable of ac-quiring a common visual direction with the foveaof the fixating eye, this anomalous interretinalrelationship is quite precise and, actually, ‘‘pointto point’’ for any given angle of strabismus.115

Finally, the fact that the angle of anomaly maychange in different gaze positions4, 74 should notbe taken in support of the previously expressednotion that innervational factors are capable ofmodifying the interretinal relationship. Whereassuch factors do influence egocentric localization,

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Examination of the Patient—III 239

as in the example of past-pointing (see Chapter20), they have no effect on the rearrangement ofvisual directions as occurring in ARC.

Quality of Binocular Vision inAnomalous Correspondence

In assessing the binocular cooperation of patientswith anomalous correspondence, one must keep inmind that their response depends on the stimulussituation presented to them. There is no doubtthat patients with anomalous correspondence arecapable of performing fusional movements trig-gered by retinal disparity. This possibility wasreported by Bielschowsky18 and subsequentlystudied and confirmed by Burian,29 Hallden,67 andothers.40, 107, 124, 140

Bagolini8 and Pasino and Maraini126 explainedthat patients with anomalous correspondence havea much larger area of horizontal single binocularvision (named the pseudo–Panum area by Bago-lini) than people with normal binocular vision.To show this, Bagolini used a form of horopterapparatus, provided with a small light on the mov-able rods, and his striated glasses. Bagolini andhis school8 demonstrated in a series of papers eyemovements (anomalous movements) in responseto horizontal and even vertical prisms in patientswith anomalous correspondence.10, 12, 41, 42 Thesemovements may fully offset the prism-induceddisparity and have been likened to fusional move-ments (vergences) in normal persons (see alsoKertesz,92 and Boman and Kertesz25).

However, they are less precise and muchslower than normal fusional vergences since themovement may take hours or days to complete.Whether their purpose is to return the prismati-cally misplaced retinal images to retinal elementsthat share an anomalous common visual directionhas not been unequivocally established. Bagolini10, 11

believes that this is generally the case but con-cedes that they may also occur independently ofthe underlying behavior of retinal correspondence.We are inclined to agree with this modified viewsince prism-induced fusional movements (prismadaptation) are not limited to patients with ARCbut can also be elicited in those with NRC.41, 139

Prism-induced anomalous movements form thebasis of the prism adaptation test which is usedby some clinicians in their surgical planning (seeChapter 26).

The presence of true stereopsis in anomalouscorrespondence is much less firmly established.

Several investigators were unable to find stereo-scopic thresholds that were higher than those inpatients with deep suppression,65, 105, 113, 127 andNelson114 concluded on theoretical grounds thatonce anomalous correspondence is present stere-opsis can no longer exist. On the other hand, therecan be no argument that gross stereopsis (usuallyless than 120 minutes of arc) is a common findingin patients with anomalous correspondence andsmall angle esotropia or microtropia73, 85, 88, 98, 102

and may occasionally even be demonstrable withrandom-dot stereograms. A gross type of depthperception can be also detected in patients withanomalous correspondence by means of the Langtwo-pencil test (see Fig. 15–8).

In addition to simultaneous perception in thepresence of a manifest deviation, as well as possi-ble restoration of some form of motor fusion,there are other functional advantages to anomalousbinocular vision as a result of ARC. Bagolini andCampos12 described patients who had a manifestdeviation while assuming a compensatory headposition. Such patients have anomalous corre-spondence in the position of torticollis and sup-pression of the deviating eye in other gaze posi-tions. Clearly, these individuals must preferanomalous correspondence over suppression andwill keep their heads turned or tilted to take advan-tage of this sensorial adaptation. Exteroceptiveand visual-motor tasks are other functions thatmay be enhanced by anomalous binocular vi-sion.39, 66 Objective evidence for increased binocu-lar activity in patients with anomalous correspon-dence over those with suppression has also beenfound. Binocular summation of VERs occurs innormal patients and in patients with anomalouscorrespondence but not when the deviated eye issuppressed.38

Prevalence

The question of how often anomalous correspon-dence is encountered in untreated patients withstrabismus cannot be answered unequivocally.Figures reported in the literature vary from 0.6%to 95%. Various factors are involved, one beingthe choice of criteria for the diagnosis of anoma-lous correspondence. Its rate of occurrence is highin infantile esotropia,14, 35, 53, 119 less common inexotropia,55 and uncommon in vertical strabis-mus.8, 60, 108

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Theories

The theory presented in this chapter is the classicone now almost generally accepted, though notnecessarily fully understood. It provides the onlysatisfactory explanation of all clinically observ-able phenomena, but some attention must be givento other thoughts on the subject, which permeatethe older and even more recent literature.

Until recently the so-called projection theoryof binocular vision (see Chapter 2) was well ac-cepted. However, it cannot explain physiologicdiplopia, let alone the phenomena of localizationin anomalous correspondence. This theory is nowonly of historical interest, as in Chavasse’s con-cept of anomalous correspondence as a pervertedbinocular reflex.

Linksz103 returned to the original rigid theory(Muller112 and von Graefe62) that normal corre-spondence is a strictly anatomical fact based onan immutable connection between distinct retinaland cortical areas. Excitations arising in specified,corresponding areas of the retinas of the two eyesare always transmitted to the same cortical area,so that the resulting cortical process, and conse-quently the sensation produced, is always a singleone. Stimulation of these corresponding retinalareas is consummated in Gennari’s stripe (the cor-tical correlate of the horopter), and stimulationof noncorresponding points is transmitted to thegranular layers in front of or behind that stripe,with resultant stereopsis.

In this theory of isomorphism (see p. 35), thereis clearly no room for the concept of commonvisual directions and it is useless to inquire howdisparate elements could acquire them. Thereforeanomalous correspondence in the classic sensedoes not exist. Phenomena observed in patientswith strabismus are explained in two ways. Insome of them, retinal rivalry ceases and one eyeis suppressed. In others, there is complete alterna-tion of foveal vision, a view reminiscent of Ver-hoeff’s replacement theory of fusion160 (see p. 35).In these patients, rivalry is also suspended, thefoveal images being consummated one at a timein the cerebral cortex. The anomalous localizationis a result of a form of panoramic vision; thepatient ‘‘sees the things where they are.’’ Linksz’stheory103 cannot account for many phenomenaobserved in patients with anomalous cor-respondence—the instability of the angle of anom-aly, monocular diplopia—and therefore it is oflittle help in clinical work.

Boeder23, 24 also assumed the immutability ofthe innate normal correspondence. He based histheory of the anomalous responses in patients withstrabismus on the observations of past-pointingassociated with paralyses of recent origin and onthe apparent movement of the surround when anintended ocular movement is not executed.

Boeder combined these observations withWalls’s findings161 on visual directions and withVerhoeff’s replacement theory160 and postulatedthat the anomalies of localization in strabismusare not the result of the assimilation of visualdirections but rather of a substitution of the visualdirection of the stimulated element by anotherretinal element, which turns the visual directionsinto an appropriate egocentric direction. This isbrought about by continued frustration of nearlyequal amounts of convergence innervation in thedeviated eye until the ‘‘response shift’’ has be-come an established conditioned reflex. Boeder’stheory is not supported by clinical facts. For exam-ple, his speculations on how the ‘‘response shift’’invariably induces an amblyopia is not in accordwith the clinical observation that not all patientswith anomalous correspondence have amblyopia.Second, and most important, this theory is basedon the unsupported assumption that a discrepancyexists between intended and executed eye move-ment in patients with comitant strabismus andthat this discrepancy causes errors in egocentriclocalization, similar to past-pointing in paralyticstrabismus (see Chapter 20).

According to Boeder,24 the lack of execution ofan eye movement for which the proper innervationhas been issued will cause a substitute directionalresponse of retinal elements in the amount ofthe angle of the frustrated rotation. In comitantstrabismus we know of no frustration of intendedeye movements as they may occur in paralyticstrabismus. Moreover, the discrepancy betweenintended and executed eye movements in cases ofparalytic strabismus of recent onset causes a shiftin egocentric (absolute) localization (see p. 29) ofvisual objects when viewed monocularly with theparetic eye. However, the essence of ARC is arearrangement of binocular relative visual direc-tions.

Postural and other functions of the motorsphere have long been resorted to by supportersof the projection theory of binocular vision in anattempt to obviate its difficulties. Motor phenom-ena, usually presented in up-to-date cyberneticterms, have been alleged to explain such anoma-

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Examination of the Patient—III 241

lies as monocular diplopia. Le Grand,101 in callingattention to past-pointing and similar phenomena,spoke of a disturbance of ‘‘motor compensation’’in strabismus or the relation between ocular rota-tion and image shift on the retina. When the ocularposition returns to normal, so does the ‘‘motorcompensation,’’ but it may coexist with the olddisturbed motor compensation and cause monocu-lar diplopia. Schober and Leisinger141 explainedLe Grand’s dynamic motor compensation in termsof cybernetics. Morgan111 proposed that some ocu-lar movements are ‘‘registered’’ in coordinatingcenters and some are ‘‘not registered,’’ dependingon whether they affect egocentric localization. Heused this concept to explain not only anomalouscorrespondence but also monocular diplopia.

A detailed discussion of these views on thepathogenesis of monocular diplopia, which can befound in a publication by Burian,34 will not begiven here, but the reader should be reminded thatmonocular diplopia can be elicited by stimulatingthe fovea of the deviated eye by means of a majoramblyoscope or with an ophthalmoscopic device,which clearly does not involve motor or posturalfactors.

Review and Summary

The phenomenon of anomalous correspondencehas been described in considerable detail, and asummary of the essential points, emphasizing theirclinical importance, may be useful. Anomalouscorrespondence consists of a reordering of thevisual directions of the two eyes so that the motoranomaly, the deviation, is fully or partially com-pensated by the sensory system. Thus anomalouscorrespondence may represent an adaptation of thesensory system to the abnormal motor situation.Adaptation to this condition requires individualadaptability as well as time. The younger the pa-tient is at the time of onset of the deviation,the more readily and more speedily anomalouscorrespondence develops. Adults who acquire adeviation maintain normal correspondence, buteven in young patients the depth of this adaptationvaries within wide limits. Different tests are re-quired to determine the depth of retinal correspon-dence. Generally speaking, tests that closely simu-late the conditions of everyday use of the eyesgive evidence of anomalous localization. Testspresenting the patient with unusual conditions ofseeing are more likely to produce a normal re-sponse, and if such tests elicit anomalous localiza-

tion, the anomalous correspondence is deeplyrooted. Similarly, if the patient is forced to use hisor her eyes in an unusual manner, made to fixatewith the usually deviated eye, or forced to acceptbifoveal stimulation, he or she may revert to nor-mal localization. Normal and anomalous corre-spondence thus may coexist and on occasion resultin monocular diplopia (binocular triplopia). Thisphenomenon, though rarely occurring spontane-ously, can be elicited artificially in patients whoseanomalous correspondence is not too deeplyrooted.

Anomalous correspondence is an attempt bythe patient to recover binocular cooperation whenthe visual axes are misaligned. To a degree, thisattempt is successful, and anomalous binocularvision is a functional state superior to that prevail-ing in the presence of suppression in alternatingstrabismus. This concept has been reinforced.79

The visual input from a suppressed eye is limitedand of no apparent benefit to binocular visionother than elimination of diplopia and confusion.

Fifty years ago anomalous correspondence wasseen as a major obstacle to restoration of normalbinocular vision and treated with great convictionby many orthoptists. It is astounding that thisattitude still prevails in some parts of the world.As a result of this therapeutic zeal many patientswith comfortable binocular vision on an anoma-lous basis regained normal correspondence andwith it, intractable diplopia. A small angle, cos-metically inconspicuous residual strabismus withanomalous correspondence is now considered bymost strabismologists and orthoptists an accept-able or even desirable endstage of therapy in in-fantile esotropia.119 It requires no further treatmentexcept for a coexisting amblyopia and affords thepatient many functional advantages of binocularvision on an anomalous basis in spite of the ocularmisalignment. According to current views, or-thoptic treatment of anomalous correspondence(see Chapter 24) is contraindicated.

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