Documenta Ophthalmologica 41,1 : 1 - 22, 1976

P A R T I.

S E N S O R I A L A N O M A L I E S IN S T R A B I M U S

(Suppression, A n o m a l o u s correspondence, A m b l y o p i a ) B. B A G O L I N I

(Modena] ABSTRACT Some concepts regarding suppression, anomalous correspondence and amblyopia are revised according to the sensorial findings obtainable from esotropic patients directly in casual seeing (with the aid of the striated glasses test) and by grading a sensorial dissociating effect (with the aid of a bar of optical filters). The following points are emphasized: 1. Suppression appears to be minimal in small angle strabismus where diplopia seems mainly to be avoided by an anomalous correspondence mechanism. On the contrary, suppression is the prevalent mechanism in large angle strabismus. 2. The anomalous correspondence mechanism may lead to a weak type of anomalous binocular vision which is easily interrupted by light optical filters or by dissociating tests. 3. The subjective space of patients with anomalous binocular vision resembles that of normal binocular vision in some aspects. 4. The development of amblyopia is interpreted in the light of these new concepts on suppression and anomalous binocular vision. 5. Postoperatively, anomalous correspondence rapidly re-adapts to the smaller angle deviation and may normalize if the deviation is completely eliminated. This is evident only in casual seeing; for a certain time, dissociating tests reveal the preoperative correspondence status. This behaviour of correspondence in casual seeing has led to attempts at normalizing anomalous correspondence by prism therapy. Newly observed sensorio-motorial obstacles, however, have been found to frequently hamper treatment in casual seeing. In c o n c o m i t a n t strabismus (provided its onset occurs early in childhood), a reorientation of the spatial values of the retinal elements of the deviated eye (called anomalous retinal correspondence) occurs in binocular vision. This newly-acquired orientation, which has been k n o w n for about a century, is generally believed to be an expression of a sensorial adaptation (Burian, 1947) t o the squint deviation in an a t t e m p t to restore a kind of binocular vision in spite of a deviated eye. This a t t e m p t , however, has rarely, if ever, been held to lead to some degree of binocular cooperation. The diplopia which w o u l d n o r m a l l y develop because of the deviation is thought to be avoided through suppression of the image received by the University Eye Clinic, Modena, Italy This work was supported in part with a C.N.R. grant No. 115.2085.3379

deviated eye. Suppression is the clinical manifestation of a synaptic inhibitory block somewhere along the visual pathways, possibly only at a cortical level, and it can be detected as scotomatous areas in the visual field of the deviated eye under binocular stimulation (see a review of the subject in Dubois-Poulsen and also in the more recent articles by Mackensen and Ravalico). Diagnosis of the state of retinal correspondence can be made by various tests; many such tests involve a comparison between the objective angle of deviation, i.e., the angle between the two visual axes, and the subjective angle, i.e., the angular distance separating the two images of an object of fixation perceived by the patient. Obviously, some artefacts have to be introduced by the test to make the patient aware of the image of the object of fixation which stimulates the deviated eye. A comparison of the objective and subjective angles reveals whether the squinting eye maintains its innate retinal directional localization (normal retinal correspondence), or if a newly-acquired directional localization (anomalous retinal correspondence) replaces normal retinal correspondence (n.r.c.). GRADING TESTS FOR ANOMALOUS BINOCULAR VISION AND SUPPRESSION Numerous tests are available for the study of binocular sensorial behaviour in squinting patients. Those normally used are the hapioscopic tests (e.g. the major amblyoscope), the red glass test, the Worth four dot test, the Hering after-image test, etc. A full description of such tests can be found, for example, in Lyle and Jackson or in Hugonnier. With these tests a diagnosis of the state of retinal correspondence and of the patient's tendency to suppress can be made. It has been noted, however, that different findings regarding the binocular sensorial relationship are obtained by different tests. This is probably due to the varying extent to which the sensorial state is altered by way o f the artefacts introduced by the various tests. The property of a test to alter casual seeing stimuli has been called 'dissociation' (Bagolini, 1961) to indicate the tendency of the test to disrupt or dissociate the anomalous binocular sensorial state reached by the patient. This anomalous sensorial state, represented by suppression and b y the change in binocular vision of the spatial directional localization of the retina of the deviated eye (anomalous retinal correspondence), does not develop abruptly. There is sound evidence that this is a sensorial adaptation to the strabismic deviation which slowly develops under the constant stimuli of casual seeing. Suppression and anomalous correspondence may, therefore, be more or less deeply rooted,

depending mainly on how long the stimuli had a chance to act on the misaligned eyes; at the beginning, they may be revealed only if the artefacts of the test used do not alter casual seeing stimuli too much, while in the long run, they may stand the dissociating effect of the test and can be revealed even by strongly dissociating tests. Concerning the evaluation of correspondence, the artefacts introduced by a test may produce a reaction indicating normal retinal correspondence if the angle of squint has been recently acquired and the anomalous retinal correspondence has not become too deeply rooted. The probability of revealing an anomalous retinal correspondence will depend, therefore, on the artefacts introduced by the test and on the depth of the anomalous correspondence itself. Generally speaking, one may say that the artefacts associated with binocular vision tests become progressively greater as the conditions of the test depart more markedly from those of ordinary casual seeing and alter the normal stimulus relationship between the two eyes (so as to make the two retinal images sufficiently different). This assumption is unprecise and provisional. Other factors besides the difference in the two retinal images may play a role; the position of the two retinal images on the retinas (see Catalino and Pannarale) seems to be an important one. So far, no systematic study has been made to find out which elementary variation of the binocular stimuli could be responsible for what we call 'dissociation'. Concerning the evaluation of suppression much the same can be said. A suppression scotoma may appear quite small when measured for instance at the major amblyoscope. There it usually manifests itself strictly at the subjective angle; with a minimal amount of dioptric displacement of the arms of the instrument no suppression of the two retinal images is observed. Suppression is certainly much greater in casual seeing (and this can be demonstrated for ex. by the use of the striated glasses) where a considerable amount of prisms may be necessary to make the patient experience diplopia. Finally, suppression scotoma can greatly vary with regard to the size according to the region of the binocular visual field stimulated and to the binocular campimetric techniques adopted to detect them. ( F o r more details about the artefacts that may change the state of anomalous retinal correspondence (a.r.c.) or suppression at various tests see Kretzschmar, 1955 and Bagolini 1967). A scale can be made of the various tests, according to their dissociating effect. Tests of common use listed according to their increasing dissociation may be the following: striated glasses, major amblyoscope, red filter and Worth four dots (the dissociating effect of the last two tests may vary according to the density of the optical filters used), negative and positive after-images. The sensorial anomalies will be weak if detected only by weak-

ly dissociating tests and strongly rooted if detected also with highly dissociating tests such as the after-images (Burian, 1947; C/ippers, 1956; Bagolini, 1961, 1967). THE STRIATED GLASSES TEST AND BAR OF OPTICAL FILTERS Not long ago a test was developed (Bagolini, 1958) which only introduces artefacts of a negligible nature. This test, the striated glasses test (S.G. test), consists of a pair of piano glasses which may be placed in a trial frame. Looking through either of these glasses, the appearance of objects viewed remains unaltered. However, when looking at a spotlight, a feeble luminous stripe can be seen crossing the light. This luminous stripe is due to almost invisible striations on the glass, and is perpendicular to these striations. A mark placed on each striated glass indicate the orientation of the luminous stripe to which it will give rise - this is called the axis of the S.G. The striated glasses are placed in a trial frame, one before each eye, and with their axes oriented at 90 ~ to each other. With the axes at, for example, 45 ~ and 135 ~ a normal subject, when fixing a spotlight, sees, binocularly, the light crossed by two luminous stripes that are perpendicular to each other, as in an X; each stripe is, of course, perceived by one eye only. The light is seen binocularly and is situated exactly at the crossing of the stripes. With a similar arrangement of the striated glasses a strabismic patient, when looking at the light (Fig. 1A) may see: 1. The light crossed by two luminous stripes, just as for a normal subject (see Fig. 1B). This indicates an anomalous overlapping of the two monocular visual fields and, therefore, a type of anomalous binocular vision. Differentiation between normal and anomalous binocular vision is evident from the fact that in the latter case, the patient shows a manifest deviation. It will be noticed that, although the image of the 'fixation light falls upon an extramacular area in the deviated eye, this light is perceived in exactly the same visual direction as its image in the macula of the fixing eye (a condition called harmonious anomalous correspondence). This type of anomalous binocular vision is almost invariably found in small angles of strabismus. 2. The luminous stripe corresponding to the deviated eye may not be perceived by the patient (Fig. 1C). This indicates complete suppression of the deviated eye; a condition almost invariably found in wide angles of strabismus. 3. The light may be perceived crossed by two luminous stripes; however, the stripe corresponding to the deviated eye may not be seen immediately around the light (Fig. 1D). This indicates a small suppression scotoma in the region of the visual field of the deviated eye, stimulated by the fixation

light.

4

A

9

light

fusion

B

(or superimposition normal or anomalous) RE

C

LE

~E

suppression of

RE

partial suppression (central) /

whith peripheral fusion or superimposition (normal or

IJ R

E

anomalous)

LE Fig. 1. Possible clinical findings at the striated glasses test. The right eye (RE) is the one which is supposed to deviate. Explanation in the text; the left eye (LE) is the the dominant.

4. The patient may experience diplopia and see two lights, each crossed by a stripe (Fig. 1E). This is a rather rare occurrence and indicates that the sensorial status of the patient is very weak. Though the striated glasses introduce a weak dissociating effect, this is strong enough to provoke diplopia. A number of other sensorial findings can be detected by the S.G. test but they occur less frequently and will not be considered here (for a review of S.G. test findings the reader is referred to Bagolini 1958; Ciancia & Bechac; Bagolini, 1967; Romano, yon Noorden, Awaya). Some care has to be taken in carrying out this test in order to eliminate any luminous source other than the fixation light from the visual field of the subject examined. To provide full binocular stimulation of the whole binocular field the room should be well lit. The cover-uncover test is always necessary to evaluate the existence of anomalous binocular vision (which is present even when a very small angle of deviation is detectable) or of normal binocular vision (when no angle of deviation is present), because weak normal or anomalous binocular vision may be disrupted by the cover test. The 'uncover' phase has to be long and

Fig. 2. Bar of red filters useful for measuring the deepness of A.R.C. (when the patient sees at the S.G. test one light crossed by two beams) or the intensity of suppression (when the patient at the S.G. test suppresses one eye).

slow so as to submit the patient to a sufficiently long binocular stimulation. In order to achieve full understar~ding of the binocular status of the patient in casual seeing, the S.G. test should be p e r f o r m e d with the help of a bar of optical filters. The one I use (fig. 2) (Bagolini, 1961) is made o f red

filters graded with conventional numbers 'from 1 (a very light, barely perceivable, red filter) to 17 (a very dense red filter). When an heterotropic patient sees a light crossed by two stripes (as in Fig. 1B), this indicates that he avoids diplopia mainly by an anomalous correspondence mechanism. In this case one may slowly slide the bar of filters, placed in front of the dominant eye, from the lightest toward the darkest filter. The lightest one which is sufficiently dark to elicit diplopia will give us an indication of the deepness of the anomalous mechanism. When the patient reacts to the S.G. test with suppression, as in Fig. 1C, the lightest filter dark enough to eliminate suppression and elicit diplopia will show the deepness of the inhibiting phenomenon responsible for suppression. Anomalous binocular vision cannot usually cope with a filter denser than No. 12 or 13, while normal binocular vision can only be disrupted by No. 16 or 17. Newly acquired normal binocular vision, as may occur in a strabismic patient under treatment, may, however, be very weak and may be disrupted to diplopia by very light filters. NEW ASPECTS OF BINOCULAR VISION IN STRABISMUS AS CAN BE DEDUCED FROM FINDINGS WITH THE S.G. TEST* The artefacts introduced by the S.G. test are minimum in comparison to the strong fusional elements it contains (fixation light and surroundings); apart from the tiny luminous stripes seen monocularly by the patient, normal surroundings are perceived intact. For this reason, the S.G. test is considered not to alter the sensorial status of the patient in casual seeing. More dissociating tests, instead of showing the real sensorial status, actually reveal the patient's sensorial reaction to the particular stimuli offered by the test. The S.G. test has, therefore, revealed some hitherto unknown aspects of the binocular sensorial relationship in strabismus and has removed some misconceptions. The conclusions drawn from the application of the S.G. test and the comparison with findings from other tests, in a large number of strabismic patients, may be summarized (from Bagolini 1967, 1970) as follows: 1. The variation of directional localization of the retina of the deviated eye (anomalous correspondence) in binocular vision frequently fully compensates the ocular misalignment so as to create a true binocular cooperation, though of an anomalous type.

What will be discussed in the following pages refers only to esotropia. Exotropia presents many common features from the sensorial point of view, but also many differences.

2. This type of anomalous binocular cooperation can be found in almost all cases of small-angle strabismus. This phenomenon is observed less frequently and suppression of the deviated eye tends to prevail in patients having a wide angle squint. In strabismus with an angle of deviation over 30 to 40 prism diopters, suppression is the common finding (see Fig. 3). F r o m a physiopathological point of view this indicates that in casual seeing the change in directional localization of the retinal elements can fully compensate the angle of deviation when this angle is not too wide. Disparate elements in the two retinae may acquire the same directional localization, thus producing an anomalous form of binocular vision, provided the disparity is n o t t o o great. When the disparity is too great (as occurs in wide angles of strabismus) anomalous binocular cooperation becomes difficult or impossible and suppression largely prevails to avoid diplopia and confusion. Under the antidiplopic mechanism o f suppression one however may still find a tendency toward a.r.c. (usually under the form of a unharmonious a.r.c.) as can be revealed at the synoptophore in which suppression is always minimal (see Fig. 3). 3. The anomalous binocular vision demonstrable in small-angle strabismus is a weak sensorial relationship in comparison to normal binocular vision. This can be easily demonstrated by means of the previously described bar of optical filters. If filters of progressive density are placed in front of one eye, anomalous binocular vision is increasingly disturbed until it breaks down and diplopia appears in a strabismic patient, often after a phase of suppression. With most traditional tests, which, as was stated earlier, introduce considerable artefacts, low grade anomalous binocular vision may be difficult to detect. Weak anomalous association is t o o easily disturbed by these tests, just as it can be disrupted by using the artefact of an optical filter in front of one eye. With many of the traditional tests, therefore, patients easily react with diplopia or suppression. This explains why most clinicians think that strabismic patients always suppress in casual seeing. It now seems, however, that suppression scotomata really occur mainly in wide-angle strabismus. Instead in small angle strabismus, anomalous binocular vision prevails, as an antidiplopic mechanism and suppression is frequently the sensorial reaction of the patient to the artefacts introduced by the test. Patients with small-angle strabismus, therefore, show an easy suppression reaction when their state of binocularity is disturbed. They frequently have no suppression in casual seeing, but nevertheless maintain a strong potential suppression. The concepts expressed in these three paragraphs are summarized in the following table i (Fig. 4). At A where no or only light dissociation is present (e.g. at the S.G. test) some sort of cortical integration of the two retinal images is possible mainly in small angle deviation. At B, suppression prevails

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• ] (UNHARMONIOUS) ] A N O MCORRESPONDENCE A L(Au) OUS

I'T]DIPLOPIA ( D }

NORMAL CORRESPONDENCE ( N )

mISUPPRESSION (S} N

$

D

Au

[ ] A N O M A L O U S CORRESPONDENCE (HARMONJOUS)(Ah) S

D

Au

Ah

N

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D

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Ah

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100 EO 60 40 MAJOR 20 &MBLYOSCOPE ANGLE OF STRABISMUS IN D~OPTERS

LESS THAN 10"

FROM 10= TO 20"

I FROM 20" TO 40'

ABOVE 40 ~

Fig. 3. Clinical findings obtained at the S.G. test, at Worth's 4 dots and Major Amblyoscope in a group of 165 esotropic patients. The same group has been divided according to the amplitude of the angle of strabismus in prism diopters, into 4 subgroups. At the S.G. test, it is quite evident that an anomalous binocular vision (anomalous harmonious correspondence) is frequent in small angle strabismus, while in large angle strabismus patients avoid diplopia with suppression. The dissociating effect of the Worth's 4 dot test makes the patient react more easily with suppression even in small angle strabismus. The dissociating effect of the amblyoscope (or Synoptophor) makes the patients react more easily with anomalous retinal correspondence of the unharmonious type. At the major amblyoscope we have considered the correspondence normal or anomalous according to whether there was superimposition, suppression, or crossing at an angle respectively normal or anomalous. The findings at the S.G. test are considered the ones closer to the realm of casual seeing, or that corresponding to the real sensorial state of the patients.

either because a greater a m o u n t o f dissociation has been i n t r o d u c e d and cortical integration b e c o m e s i m p o s s i b l e or because the angle o f strabismus is t o o wide; in fact, in wide angle deviation, the prevalent m e c h a n i s m to avoid diplopia seems to be suppression. If an even greater a m o u n t o f dissociation is i n t r o d u c e d (for e x a m p l e b y dense red filters) suppression, either provoked or s p o n t a n e o u s , decreases till diplopia appears (C).

Ah

STRABISMUS

STRABISMUS

(with small angle of deviation)

(w th ar~e angle of deviation)

m ,,c

CORTICAL INTEGRATION OFRETINAL IMAGES POSSIBLE

ABNORMAL BINOCULAR VISION

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CORTICAL INTEGRATION IMPOSSIBLE PREVALENCE OF INHIDITION PHENOMENA

CORTICAL INTEGRATION IMPOSSIBLEWITH TOTAL DISSOCIATION OFTHE VISUAL FIELDS AND DISAPPEARANCE OFTHE INHIOITION PHENOMENA

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SUPPRESSION strong in the deviated eye

slight in the deviated eye

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