Ophrhal. Ph-vsrol. Opr., Vol. 5 . No. 4. pp. 357 ~ 368. 19R5. Printed in Great Britain.

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c 1985 British College of Ophthalmlc Opticians (Optomerriris)

ANOMALOUS RETINAL CORRESPONDENCE - A REVIEW

J . A. M. JENNINGS* Department of Ophthalmic Optics, University of Manchester Institute of Science and Technology, PO Box 88, Sackville

Street, Manchester M60 lQD, U .K.

(Received 7 October 1984, in revised form 20 February 1985)

Abstract-The theories and characteristics of anomalous retinal correspondence (ARC) are critically reviewed and a classification of ARC is proposed which attempts to reconcile various aspects of the different theories. I t is suggested that ARC in microtropia, and perhaps some small-angle squints, is a cortical adaptive mechanism, whereas squints with a larger and more variable angle have ARC with different characteristics, which are better explained by the motor theory.

INTRODUCTION Anomalous retinal correspondence is a difficult and confusing topic because of the bewildering diversity of strongly held and apparently contradictory state- ments found in its literature. The main cause of this confusion and disagreement is seen in Fig. I , after Bagolini (1967). A total of 165 patients are sub- divided in terms of the size of their strabismic angles and then each patient’s retinal correspondence is evaluated by four methods. The apparent binocular status is extremely variable and the observed inci- dence of anomalous retinal correspondence depends on the method of investigation as well as the nature of the squint. Additionally, the interpretation that investigators tend to put on their data is influenced by whichever theoretical basis for anomalous corre- spondence they prefer. This makes i t necessary to first consider the main theories of anomalous correspondence: the binocular performance in strabismus is then discussed.

Definitions Anomalous retinal corr‘espondence (ARC)

describes the condition in which a control mark seen only by the deviating eye of a squinter is perceived in the binocular visual field in a direction different to that to be expected on the basis of normal retinal correspondence (NRC). The spatial localization of the deviating eye appears to have shifted so as to counteract the effect of the ocular deviation. This shift in directional localization is called the angle of anomaly.

I f the angle of anomaly is equal to the angle of the squint then the anomalous correspondence com-

*Fellow of the British College of Ophthalmic Opticians (Optometrists).

pensates exactly for the squint and is described as harmonious anomalous retinal correspondence (HARC).

If the angle of anomaly is greater than zero but less than the angle of the squint, then the anomalous correspondence is described as unharmonious anomalous retinal correspondence (UN-HARC).

I f the angle of anomaly is in the “opposite”, i.e. non-compensating, direction the correspondence is described as paradoxical anomalous retinal correspondence (PARC).

THEORIES O F ANOMALOUS RETINAL CORRESPONDENCE

The Innate Theory of anomalous retinal correspondence

The earliest accounts of ARC are credited to de la Hire (1730) (see Hallden, 1952) and Muller (1826) (see Donders, 1864). I t was presumed to be secondary to a congenitally misplaced fovea causing the eye to apparently squint. Hering (see Duke-Elder, 1973) followed de la Hire and Muller in considering retinal correspondence to be innate and immutable. Hence anomalous correspondence reflected a congenital anomaly and was untreatable. Support for this view in at least a proportion of cases was offered by Adler and Jackson (1947) who suggested that, in some large-angle, non-accommodative squints, congenital anomalous correspondence is the cause rather than the result of the squint. Similarly, Bedrossian (1954) proposed congenital anomalous correspondence as the reason for the failure of normal correspondence to assert itself following surgical re-alignment of the visual axes.

Brock and Givner (1954) note that an after-image at the fovea of the dominant eye is, when the dominant eye is occluded, spatially localized as

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N S D U H N S D U H N S D U H

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1.ig. I . The apparent retinal correspondence of 165 strabismic subjects, after Bagolini (1967). Each \ubject’s binocular status was assessed by four methods, as indicated on the left hand side of the figure. The subjects were divided into four subgroups according to the size of the strabismus. The heights of the hnrs indicate the percentage incidence of the various binocular conditions. N , normal retinal correspondence; S, suppression; D, diplopia; U, unharmonious anomalous retinal correspondence; H, harmonious anomalous retinal correspondence. In the after-image test no distinction was made between harmonious and unharmonious anomalous retinal correspondence, so the incidence of both conditions is

combined (U + H).

though i t is at the fovea of the squinting eye. They conclude that “retention of the fovea- fovea relationship in cases of unilateral strabismus of very early onset points to an innate character of retinal correspondence”.

The fixed and anatomical nature of retinal correspondence was vigorously argued by Verhoeff (1935, 1938). However, his “New Theory of Binocular Vision” (1935) questioned not just the flexibility of retinal correspondence but also its purpose. In his “replacement” theory he proposed that correspondence was not to subserve “fusion”, a concept he denied, but to relate the points in each retina which alternate in perception and provide a “unified” binocular image. This idea, that the purpose of correspondence was to direct suppression to a point on one retina when the corresponding point was stimulated in the other, was to have a profound effect on the later theories of anomalous correspondence, e.g. Travers (1938, 1940) and Boeder (1964). Verhoeff (1938) himself stated that squinters have no correspondence (p. 666) because

the regions of anomalous binocular vision he detected (p. 670) were substantial areas rather than the point-to-point relationships his theory led him to expect. Although he conceded that squinters had anomalous projections he denied their anomalous correspondence. The complexity of Verhoeffs reasoning makes Burian (1947, p. 625) comment that “it is difficult for one well-versed in the subject to follow Verhoeff‘s paper (1938). For one not intimately acquainted with the subject it is probably impossible to understand it.”

The Adaptive Theory of anomalous retinal correspondence

The alternative view that the retinal correspon- dence changes as a sensory adaptation to the squint dates from Steinbruck (1812) (see Hallden, 1952) and the clinical observations of von Graefe (1858) (see Duke-Elder, 1973).

The theory proposes that the “Local Sign” (Walls, 195 l a , pp. 78 - 82) of the anatomically correspond- ing points is learned in early life and that within this

Anomalous retinal correspondence-a review 359

learning period there is the possibility of some adaptive modification in correspondence. The most convincing apologist of the adaptive theory was Burian (1947) whose carefully argued thesis forms the basis for the present conventional view of ARC as a sensory adaptation. “The anomalous retinal correspondence represents thus a process of adap- tation of the sensorial to the anomalous motor conditions; i t consists of a shift of the visual direc- tions of one eye relative to those of the other eye” (p. 506). “Also it is a slow process and at first the relationship is not very deeply rooted” (p. 367).

Travers’ Theory of anomalous retinal correspondence

Early investiators assumed ARC to be harmonious (Hallden, 1952) and this was the usual result found with methods based on Tschermak’s Kongruenz- apparat (Burian, 1947; Bagolini, 1967). Subsequently the development of the synoptophore and its almost universal use in the second quarter of this century led to an accumulation of quite different clinical experi- ence and data. These suggested that squinters habitually suppressed, and that when the suppression was overcome on the synoptophore, they demon- strated either NRC or UN-HARC. Harmonious anomalous retinal correspondence was rarely found (Hallden, 1952; Pickwell, 1963; Lyle and Wybar, 1967; p. 211).

The late 1930s were dominated by Verhoeffs (1935) Replacement Theory of Binocular Vision, e.g. “the great authority which every article by this distinguished writer carries” (Burian, 1947, p. 340). Travers’ (1938, 1940) theory of ARC was a product of this theoretical background and synoptophore- based clinical observations. His objective was to explain the more frequent detection of UN-HARC than HARC and to do this within the framework of a general acceptance of Verhoeff‘s theory of binocular vision. He proposed that the confusion and diplopia of a squinter with NRC was relieved by suspension of the “replacement” mechanism, hence a suppression scotoma developed in the deviating eye. He then argued that a point adjacent to the now suppressed fovea of the deviating eye next achieved an anomalous correspondence with the fovea of the fixing eye. This unharmonious correspondence still potentially produced diplopia and confusion, so this in turn was suppressed. The procedure continued with the anomalously corresponding point moving across the retina until it became harmonious. This was envisaged as a slow process, which may not actually be completed. Thus most patients would

exhibit UN-HARC when examined. The influence of Verhoeff meant that Travers did not expect ARC to provide a useful form of binocular vision. Rather his theory (Travers, 1938, p. 603) was that a change in retinal correspondence would allow suppression to be directed to the retinal regions in the deviating eye which, i f not suppressed, would give rise to diplopia and confusion. The fact that patients who demon- strated UN-HARC on the synoptophore did not complain of diplopia under conditions of casual seeing was taken as support for the theory-it showed that the ARC was directing suppression in a useful manner and hence fulfilling its objectives. Travers’ essentially adaptive theory was widely accepted and still has considerable influence (e.g. Cashell and Durran, 1980, pp. 54-55). I t was plausible because it “explained” the apparent facts and could be presented as an extension of Verhoeff‘s already accepted theory. The clinical observations of Ronne and Rindziunski (1953) provided support for Travers with their five-stage “clinical classifications” where cases are described as progressing from NRC to total suppression, UN-HARC and finally “a constant angle of anomaly identical or nearly so with the objective angle”.

Linksz (1952) doubted the existence of ARC and was unconvinced (pp. 567-575) by the active suppression mechanisms proposed by Travers (1938). He thought that the apparent scotomata were more likely to be a result of normal binocular rivalry, biased by the relative “impressiveness” of the stimuli. His own experience was that young amblyopes could not reliably localize in the synoptophore (p. 557). This led him to distrust claims for ARC based on synoptophore findings. The only ARC that he was prepared to take sufficiently seriously to refute in detail (pp. 562 - 567) was that ascribed to the equal acuity alternator. The opinion at that time was that ARC was most common in alternating squints, e.g. Ad:er and Jackson (1947) said that “eighty-three percent of persons with alternating squint have anomalous correspondence”. Bedrossian (1954) concluded that 64% of early-onset alternating esotropes have ARC. Linksz (1952) was well aware that stimuli falling successively on the alternator’s foveae are localized in their different, and correct, directions in visual space, even in the absence of any eye movement. However, he points out that this phenomenon does not require ARC, rather the absence of any correspondence and alter- nating monocular perception. Today few would disagree with Linksz’s reservations about the assessment of sensory status on the synoptophore

360 J. A. M . Jennings

(e.g. Bagolini, 1967) or with his explanation of the perception of the alternator. However, simply because he did restrict his considerations to these particular circumstances, his general rejection of the possibility of ARC in any squint is a little dubious.

Burian (1947) did not rely exclusively on the synoptophore for diagnosis and he frequently found HARC in squinters. He was unconvinced by Verhoeff‘s replacement theory and unhappy about his rejection of the existence of “anomalous correspondence adapted to the angle of the squint” (p. 628). Burian’s clinical experience that “I have never observed gradual changes in the angle of anomaly” (p. 620), that squinters apparently have measurable fusional reserves (Burian, 1941) and the existence of post-surgical competition between NRC and ARC (Burian and Capobianco, 1952), convinced him that ARC was a positive asset to the patient rather than just a means of organizing suppression. The universal observation that the apparent correspondence depends on the method of investi- gation suggested to him that the more deeply established the sensory adaptation becomes, the more techniques will indicate its presence. Hence the depth of the sensory adaptations can be assessed on the basis of which apparatus will and which will not detect it. I t is assumed that the longer standing and more constant the squint, the “deeper” will the ARC become established (Mallett, 1970b, 1975; Bagolini, 1976a, 1982).

The exact mechanism by which ARC becomes established is not considered by Burian (1947). Walls (1951b. p. 140) proposed “a whopping slippage in Area 19” of the same nature as that which he presumed subserves normal fixation disparity and Panum’s Areas. Bagolini (1967, 1976a) suggested the facilitation of an anomalous cortical pathway. Electrophysiological investigations have produced some support for this view. Shlaer (1971) raised kittens wearing 4A vertical prisms. A compensating shift in the mean disparity sensitivity of 19 cortical cells was found. This shift was slightly less than 4A, perhaps indicating either a contribution from vertical fusional eye movements or that “the disparity of 4A may exceed the limit set by the pre-existing cortical structure. If the mechanism of cortical plasticity during maturation acts only by selecting synapses for preservation from a set of synapses present at birth without establishing new contacts, then such a limit must exist”.

Shinkman and Bruce (1977) performed a similar experiment, only this time a cyclo-disparity of 16” was introduced between the eyes. In this case an

almost perfect compensatory shift was found. A larger disparity of 24” was found to be more disrup- tive of binocularity, perhaps again indicating a limit set by the cortical structure. [The results of Smith et al. (1979) with 15A base-out prisms are less con- vincing because of the uncontrolled convergence. I On the basis of these findings a genuinely adaptive ARC seems to be a real possibility in small-angle squints. An alternative adaptive theory was proposed by Nelson (1981). After authoritatively reviewing the neurophysiology of binocular vision he notes that disparity detectors have a roughly normal distri- bution centred on the horopter (e.g. Bishop, 1981). The predominance of zero-disparity detectors, i.e. the “modal tuning”, establishes what Nelson designates the “resting state of correspondence”. However, if a stimulus selectively and powerfully stimulates non-horoptal disparity detectors then “the most active disparity tuning within a locale is treated by the visual system as the modal tuning and is the disparity value which will be perceived to have common visual directions. In other words, if the response to a disparity i s strong enough it will be fused” (Nelson, 1981, p. 38). “The machinery of disparity detection bestows the cortex with the capacity to support a multiplicity of correspondence states and it is argued that sensory fusion mechanisms govern which state will be expressed at any moment” (Nelson, 1981, p. 5 ) .

Less elegantly argued but similar suggestions have been made independently by various authors, e.g. Stanworth and Da Cunha (1959), Bagolini (1967), Crone (1969), Crone and Hardjowijoto (1979), Goersch (1979) and Friedburg (1981). However, the conventional view is that although the disparity mechanisms permit sensory fusion of disparate stimuli, rather than this leading to a change in correspondence, the modal disparity is subsequently relieved by motor fusion (Schor and Ciuffreda, 1983). However, Goersch (1979) does claim that in subjects with a clinically stable fixation disparity there is eventually a shift in correspondence.

Behavioural work (Olson, 1980) confirms the possibility of ARC in kittens but it is interesting to note that Olson is sceptical of the available electro- physiological data.

Motor theories of anomalous retinal correspondence An adaptive process implies a “learning” period in

which adaptation becomes progressively more estab- lished and subsequently there should be a temporary after-effect when the adapting conditions are removed. Though such effects have been observed in

Anomalous retinal correspondence-a review 361

ARC, e.g. monocular diplopia (Burian and Capobianco, 1952; Duke Elder, 1973), the findings are frequently different. Patients often show HARC continuously despite the angle of squint changing from distance to near, looking up and down (Mallett, 1967; Bagolini, 1976a) or with and without spectacles (van Noorden, 1967). The presence or absence of ARC in different instruments may not reflect “depth” of ARC as much as whether the instrument presents the threat of diplopia and confusion which forms the stimulus to ARC. Also the fusional (Kerr, 1980) and accommodative (Daum, 1982) demands of the particular instrument have been found to influence the angle of anomaly.

These unsatisfactory aspects of ARC as an adaptation led Morgan (1961) to review critically Burian’s (1947) adaptive concept and propose an alternative motor theory. The concepts underlying Morgan’s theory had been considered by Chavasse (1939, p. 383) and particularly Walls(1951a-c). The theory emphasizes the twin components of ego- centric spatial localization. Oculo-centric localization refers to the visual direction associated with a particular retinal (and cortical) point. This direction is not absolute but relative to the ego-centric localiz- ation attributed to the fovea of the eye at that time. As Walls (1951b, p. 133) succinctly puts it : “the material on a television screen is organized not with reference to the location of the receiver, but with reference to the location of the camera. Area 17 is the screen, but the eye is the camera”. That is, regions in Area 17 do not of themselves have ego-centric local- ization, only oculo-centric localization. The source of the eye-position information which converts an oculo-centric direction into an ego-centric direction is controversial. Chavasse (1939, p. 355) quoted Sherrington and suggested proprioceptive feedback from the extra-ocular muscles. Some psychophysical and electrophysiological investigations have given support to this (e.g. Skavenski, 1972; Buisseret and Maffei, 1977). In a series of 50 alternating esotropes Schiavi et a/. (1969) report a consistent reduction in angle of anomaly following surgery and several days occlusion. The occlusion was to prevent any visual influences. They attributed the change in correspon- dence to the modification of proprioceptive feedback caused by the surgery. IBagolini (1976a) was sceptical and considered the results more an indication of the plasticity of ARC than a demonstration of the role of proprioception. I The more widely accepted source of (extra-retinal) eye-position data is that postulated by the efference copy or outflow theory and that this information comes from the effort of will put forth

in moving the eyes (Helmholz, 1866, see Skavenski, 1972). Despite the general acceptance of the outflow theory and its plausibility, with respect to passive eye movements and after-image localization, there is accumulating evidence that abnormal proprioceptive feedback of one eye, even in the absence of visual inputs, is sufficient to disrupt the binocularity of the cortex and lateral geniculate nucleus (LGN) (Fiorentini and Maffei, 1974; Brown and Salinger, 1975; Maffei and Bisti, 1976; Maffei and Fiorentini, 1976, Salinger et a/., 1980). However, some experi- mental investigators have failed to confirm this (Van Sluyters and Levitt, 1980; Berman ef a/., 1979). Stone (1983, p. 341) discusses these data and observes that the LGN effects are quite different to those from lid suture, and they occur in adults not susceptible to lid suture effects. Salinger ef a/. (1980) propose that the effects are not caused by loss of sensory input but by loss of the normal kinesthetic input from the extra- ocular muscles. The whole LGN is affected, not just certain layers. Nelson (1981, p. 19) emphasizes that “with surgically induced strabismus rather than occlusion, damage to the X-visual sub-system may be relatively greater. This seems to be the case with strabismus induced either by severing the extra- ocular muscle or by paralysis through nerve section, which would also eliminate proprioceptive feedback from the muscles”. Berman ef a/. (1979) find no comparable effects in the cortex, suggesting that binocular competition is not a factor.

The source of the eye-position information is not crucial to Morgan’s theory, although he seems to assume “outflow”. The important factor is that the innervation pattern of the extra-ocular muscles gives the potential for a change in the correspondence by influencing the correction from oculo-centric to ego- centric localization. He suggests that vergence inner- vation does not change ego-centric localization, therefore, an accommodative squint should not be accompanied by ARC whereas a concomitant squint due to an anomaly of the version mechanisms would be expected to have ARC. “Thus anomalous corre- spondence might depend not on sensory adaptations to a squint but rather on whether the basic under- lying innervational pattern to the extra-ocular muscles was one which “registered” itself in consciousness as altering ego-centric direction” (Morgan, 1961, p. 139). Despite the interesting results of monocular immobilization experiments (Fiorentini and Maffei, 1974; Brown and Salinger, 1975; Maffei and Bisti, 1976; Maffei and Fiorentini, 1976; Salinger et a/., 1980), i t is not obvious exactly how the correction from oculo-centric to ego-centric

362 J . A. M. localization can be different for each eye. Rather than seeing this as a difficulty, Walls (1963) speculates that ARC may be a regression to a more primitive form of binocular vision. “When we have said all this, we have really also described what happens in the lower vertebrates with total decussation, when they perform their independent eye movements” (p. 330). Alternatively, Pickwell (1980) and Reading (1983, p. 329) have proposed that inhibition of the Y-system of the squinting eye would account for many of the characteristics of ARC.

However, Morgan makes it apparent that the explanation of ARC need not necessarily be sought in a neural pathway adaptation but in a change in the sensed position of the squinting eye. The immediate attraction of this approach is that it has none of the restrictions to small-angle squints which were apparent in adaptive ARC and offers the possibility of an instant change in correspondence with changed conditions. Unfortunately, the impressive prediction that ARC is less likely in accommodative than in non-accommodative squint has not been clinically substantiated.

An alternative form of “motor theory” has been vigorously argued by Boeder (1964, 1966, 1967, 1978). Starting from the observation that the “past- pointing” exhibited by a recent palsy is an example of a modification of ego-centric localization, Boeder (1978) proposes that a “response shift always results when, for some reason, the eye is in a position different from the one called for by ocular inner- vations’’. This theory is difficult to reconcile with other recent work since it is based on the “replacement” assumptions of Verhoeff‘s (1935) theory. Thus Boeder’s view of the purpose and potential of ARC is rather different from either Burian or Morgan. Boeder (1978) comments on his theory: “few were convinced, many could not see any difference, and others were negative”.

Sittiitnary Excluding a rare congenital anomaly, the innate

theory of ARC is not compatible with clinical observations. The adaptive theory is convincing for a proportion of small-angle squints of constant angle and long duration. However, the motor theory offers the promise of an ARC which varies with the sensed positions of the squinting eye.

MEASURABLE CHARACTERISTICS O F ANOMALOUS RETINAL CORRESPONDENCE

Stereopsis in anomalous retinal correspondence The authorities show a n uncharacteristic

Jennings

unanimity about the absence of stereopsis in ARC I e.g. Bielschowski, Adam, Mugge and Tschermak, see Moncrieff (l929), Verhoeff ( I 938), Travers (1938), Burian (1947), Hallden (1952), Ronne and Rindziunski (1953), Boeder (1966, 1967, 1978), Bagolini (1976a, 1982), Burian and von Noorden (1974, p. 262) and Nelson (1981, p. 82)l. Following the development of Bagolini-striated glasses in 1958 (Mallett, 1967) and increased use of the visuscope (von Noorden, 1959), diagnosis of ARC in small- angle squints became practical. Helveston and von Noorden (1967) described a “newly defined entity”, microtropia, a small squint which shows no movement on the cover test because the ARC and eccentric fixation points coincide. Using the Titmus test, stereo acuities of 100-s were typical and two subjects had 20-s thresholds. Other studies, e.g. by Naylor and Stanworth (1959), Epstein and Tredici (1973) and Herison and Williams (1980), demon- strated Howard-Dolman and, in the latter two, Titmus-stereo thresholds vastly better than chance or monocular performance in a variety of small-angle squinters. The most recent of these studies compared the monocular and binocular Howard - Dolman thresholds of 14 squinters. Subjects with squints of < 8A generally showed dramatically enhanced binocular performance and stereo thresholds of 10-20-s. (Normals averaged 6-s on the same apparatus.) The Titrnus-stereo test gave 40- 80-s thresholds on these small-angle squinters. A similar difference in threshold between Titmus and Howard - Dolman was noted by Mallet (1970b). A difficulty with the Titmus test is its unreliability as an indicator of low-grade stereopsis in the 800 - 200-s range. The lateral displacements of the stimuli are detectable monocularly when seen through the polaroid glasses (Simons and Reinecke, 1974; Cooper and Warshowsky, 1977; Henson and Williams, 1 980).

Reinecke and Simons (1974) and Hill et al. (1976) reported positive responses, by small-angle squinters, to random-dot stereograms of several hundred seconds disparity. In what claims to be the most careful study so far, Cooper and Feldman (1978, 1981) could find no random-dot stereopsis in squinters of any kind, including microtropes (Helveston and von Noorden, 1967). They stress the problems of diagnosis and angle variation in small squints and suggest that some of the reported cases of random-dot stereopsis, in fact, had no squint at all at the moment of testing. (The frequent use of the term “microtropia” to describe any squint of < 5 ” , as proposed by Lang (1969), is an additional compli-

Anomalous retinal correspondence-a review 363

cation when comparing data from different sources.) The evidence strongly suggests that Howard -

Dolman and Titmus stereopsis of better than 100-s is present in at least some strabismics. This ability does not seem to be restricted to true microtropes, as implied by Helveston and von Noorden (1967), but also includes some small-angle squints which are detectable on the cover test (Henson and Williams, 1980). Random-dot stereopsis provides a “harder stereopsis task” (Frisby et al., 1981, p. 212) than Titmus and there is considerable doubt if strabismics of any sort can succeed in such tests (Cooper and Feldman, 1978, 1981).

In large-angle squints an extensive area of sup- pression in the deviating eye is usually found (Bagolini, 1967; Mallett, 1970b). No stereopsis is possible in this central binocular field but some coarse peripheral depth perception has been found in such subjects (Sireteanu, 1982). A “motion in depth” stimulus was used, where each eye’s target was moved laterally in opposite directions. The resulting binocular effect is of a stimulus oscillating in depth. Exactly how this sort of dynamic stimulus relates to the more usual static display is very complex (e.g. Cynader and Regan, 1982).

I t is interesting to speculate about the relationship between small-angle squints with stereopsis and the physiologically adaptive ARC demonstrated in prismatically dissociated kittens by Shlaer (1971) and Shinkman and Bruce (1977). The clinical stability of microtopia does suggest a genuine adaptive basis for the ARC.

Depth of anomalous retinal correspondence The concept of ARC becoming “deeper” or

“more deeply ingrained” was popularized by Burian (1947, p. 367). “It (ARC) is a slow process, and at first the new relationship is not very deeply rooted. At this stage, it will be present only under normal conditions of seeing and tests made under such conditions will more easily elicit it. But as this new anomalous correspondence takes deeper roots, i t will push the normal relationship of visual directions more and more into the background. Eventually it may become so firmly established that i t is impossible to elicit the innate, now dormant, normal retinal relationship in tests in which one aims at the most direct determination of this primitive anatomically determined relationship”. Thus apparatus where a normal binocular input is prevented (Mallett, 1970b) and where the two foveae are preferentially stimulated (Levinge, 1954; Pickwell and Sheridan,

1973; Nelson, 1981, p. 50) will be a very inefficient means of detecting ARC.

On this basis it is possible to grade ARC in terms of the nature of the stimulus conditions under which it persists. A rough hierarchy of apparatus can be developed with the Bagolini-striated glass as the most sensitive device followed by the Stanworth synopti- scope (Mallett, 1970a), the synoptophore and after- image tests (Mallett, 1970b; Bagolini, 1976a). Alternatively, the vision of the squinting eye can be gradually impaired with a filter bar. The darkest filter with which ARC is retained is taken as a measure of the “depth” of the anomaly (Bagolini, 1976a). On an instrumental or filter bar basis, Mallett (1970b, 1975) has suggested classifying ARC in depth so as t o optimize treatment strategy. In the stereopsis investigation of Henson and

Williams (1980) the “depth” of the ARC of their strabismic subjects was measured with a neutral- density filter bar. The subjects with the more deeply ingrained ARC tended to have the better stereopsis.

Criticism of the whole concept of “depth” has been raised principally by followers of the motor theory for whom “depth” is unwelcome evidence of adaptation. Flom and Kerr (1967) observed that all methods of diagnosis show considerable variability and in their study they took care to allow for the estimated error of each method. Their statistical analysis failed to show a significant hierarchy of tests. This study did not include the Bagolini-striated glass and its conclusions relied heavily on the finding of similar sensitivity for the synoptophore and after- image tests. However, two-thirds of the 93 subjects showed the same diagnosis on four out of the five methods employed. A similar investigation by Johnston (1970) included the Bagolini lens and came to the same conclusion of being unable to support the “depth” concept. Unfortunately all the patients in this investigation “had previously shown an anomalous correspondence with either the synotophore or after-image tests” (p. 42). Thus the range over which the Bagolini glass might be expected to show its greater sensitivity had been excluded.

Sensory and motor fusion in anomalous retinal correspondence

Normal binocular visual space is usefully described by the longitudinal horopter and Panum’s fusional space. The horopter in ARC has proved very difficult to demonstrate experimentally, defeating even Ogle (see Flom and Weymouth, 1961). Flom and Weymouth (1961) were the first to report success

3 h4 J. A. M . Iennings

using an alternate flashing “phi-phenomenon” method. Subsequent horopter experiments have been ably reviewed and analysed by Mallett (1973) and in greater detail by Reading (1983).

Reading (1983) acknowledges the sparsity and variability of the available data but favours, at least over the central binocular field, a horopter in ARC qualitatively similar to that of normal binocular vision. Flom (1980a,b) vigorously defends his results which have a marked “notch”, convex towards the subject, in the region between the crossed visual axes of the esotrope, a feature also found by Johnston (1971). Flom (1980a,b) attributes this peculiarity to the stimulation of both nasal retinas by objects in this region. He also observes that it indicates a variation in the angle of anomaly in different parts of the field, a possibility considered by Hallden (1952) and Bagolini (1967).

The different forms of horopter found may be a result of the horopter criterion used (Reading, 1983, p. 221). Flom and Weymouth’s (1961) phi- phenomenon apparatus evaluates the “common visual direction” horopter whereas Bagolini and Capobianco (1969, Pasino and Maraini (1966) and Bagolini (1967) use both the “apparent fronto- parallel plane” and the “diplopia detection” criteria. Whatever the exact shape of the horopter, there is general agreement that the locus of the horopter is much less precise and the anomalous fusional space is much larger than that of normal binocular vision (Bagolini and Capobianco, 1965; Pasino and Maraini, 1966; Bagolini, 1967).

The horopter and fusional space of ARC is evidence for sensory fusion and raises the possibility of anomalous motor fusion. Burian (1941) and Hallden (1 952) described anomalous fusional movements but both have been criticized (Maraini and Pasino, 1964; Mallett, 1970b) for a failure to measure eye position. The basic difficulty in these experiments is to distinguish between a fusional movement of the eye and maintenance of anomalous binocular vision by a change in the angle of anomaly. Maraini and Pasino (1964) ingeniously tried to separate the two possibilities. An after-image produced around the fovea of the deviating eye was located with respect to a fixation light viewed binocularly through Bagolini-striated glasses. The introduction of 6A B.O. (base out) before the deviating eye has two possible effects if anomalous binocular single vision is maintained. I f the after- image to fixation-light separation remains constant, then a compensatory fusional movement has occurred. I f the after-image to fixation-light separation decreases by 6A then a compensatory

change in the angle of anomaly has occurred. The eleven subjects unfortunately gave results of less elegance than the experimental design. Three subjects showed compensatory fusional movements, four showed a compensatory change in the angle of anomaly and four a combination of fusional movement and change in angle of anomaly. All of them retained anomalous binocular single vision throughout. Similarly diverse results were found by Johnston (1970) and Kerr (1980). The enigmatic nature of these anomalous fusional movements had been noted earlier by Alpern and Hofstetter (1948) who emphasized the remarkable slowness of these eye movements. Alpern had a 14A esotropia with HARC; 18A B.O. was placed before his eyes. After about 30 min the squint angle increased to 30A. The full 32A, a complete neutralization of the prism, was only achieved after about 2 h. No diplopia was experienced at any time, perhaps indicating a quick response by a change in the angle of anomaly which is slowly relieved by a change in eye position

Bagolini (1976b, 1982) confirms the slow nature of “anomalous fusional movements” in many patients and comments (1976b) on their lack of precision - “anomalous movements have an angular displace- ment which is frequently lower than the prismatic power of the base-out prism applied”. Bagolini (1976b, 1982) points out that the retention of anomalous binocular single vision under such circumstances does not necessitate a change in the angle of anomaly but more simply a utilization of the large pseudo-Panum’s Areas and an anomalous fixation disparity mechanism.

Schoessler ( 1 980) used infra-red eye-movement recording to study the response to potentially fuseable bar targets, presented haploscopicly on the fovea of the dominant eye and to either side of the ARC point in the deviating eye. A vergence movement in the appropriate direction to maintain ARC was usually obtained. (The size of the move- ment was not measured.) The conclusion was drawn that disparity-induced vergence movements can be initiated by ARC. Kerr (1980) proposed that the fusional convergence innervations which produce the eye movement have a component that also alters the anomalous correspondence, but the work of Kenyon et ol. (1981) disagrees with these findings. They find no evidence of disparity-induced vergence move- ments in strabismic subjects with real targets moving in depth. The eye-movement response observed can be attributed entirely to accommodative-vergence effects, covering the deviating eye had no effect on the eye movement.

However, Daum (1982) presents data showing that

Anomalous retinal correspondence-a review 365

the angle of anomaly can co-vary with changes in the squint angle produced by forced accommodation through minus lenses. IA result which is rather at odds with the predictions of the motor theory (Morgan, 1961).1 Interpretation of this data is made difficult by the choice of subject who was a 50A exotrope with well-established ARC. Most authorities, e.g. Bagolini (1967, 1976a), would agree that this is an unusual case.

Burian and von Noorden (1974, p. 262) state decisively that “the ability of patients with anomalous correspondence to respond with fusional movements is not in doubt”. Bagolini (1967, p. 359) is less certain. “The different speed of the increase of the muscle tonus in comparison to normal fusional movements may point to a mechanism of a different nature. 1 would then cautiously accept the term of ‘ fusional movements’. ”

The time scale of these “anomalous fusional movements (several minutes)” is more typical of changes in tonic convergence rather than normal fusional convergence movements ( - I-s) (Schor and Ciuffreda, 1983, p. 157) and the effects are very reminiscent of prism adaptation in the normal subject (Carter, 1960; Henson and North, 1980). The “eating up” of prism by strabismics (Bagolini, 1976b; Mallett, 1979) may be a further aspect of this effect.

Other views that “anomalous fusional move- ments” are to maintain a suppression scotoma in the most effective position or that they are a result of “horror fusionis” are discussed and rejected by Hagolini (1976b).

THE CLASSIFICATION O F ANOMALOUS RETINAL CORRESPONDENCE

Consideration of the theories and alleged characteristics of ARC leads one to concur with Duke-Elder’s (1973, p. V ) observation. “Jampolsky remarked with truth that the world would be a happier place if no one had thought of anomalous retinal correspondence”.

The “unhappiness” caused by ARC is mostly a consequence of the various investigators having quite different concepts of the purpose and potential of ARC. Most early workers and the modern followers of Verhoeff and Travers envisage ARC as providing a means of organizing regional suppression to avoid diplopia; not as a means of providing binocular single vision to squinters. Burian (1947), Bagolini (l967), Mallett (1970b) and the contemporary “adaptive” school see ARC as capable of providing an inferior form of binocular vision extending in

some cases to useful stereopsis. They stress the importance of potential diplopia as the stimulus for ARC. They would expect that only a minority of patients have ARC so well-established that it persists when the problems it exists to solve are no longer present, e.g. under haploscopic stimulus conditions. They also stress the proximal effects on accom- modation and convergence of a restricted and contour-deficient visual environment (Bagolini, 1967). These factors lead to apparent unharmonious ARC in synoptophore investigation of subjects who have harmonious ARC under the “free space” conditions of the Bagolini-striated glass.

There is a tendency for the motor school to undermine their own arguments by ignoring instru- mental effects because they are suggestive of “depth of ARC” with its implicit support for the adaptive theory. For example, the excellent work of Schoessler (1980) appears dubious to the dedicated “adaptive” reader because of the lack of concern with which three of the four esotropic subjects (16-20A deviations) are designated as having unharmonious ARC, one of these, paradoxical ARC. The “adaptive” reader would not doubt that such results can be obtained on a haploscope but would feel that such a diagnosis is only a true reflection of their casual seeing status if constant diplopia is a symptom. The inclusion of the results with a Bagolini-striated glass on these patients would clarify the diagnosis. I t may be that the change in corre- spondence from one apparatus to another is not a result of “depth” of adaptation, but rather a response to the changed level of convergence innervation produced by the different stimulus conditions. Indeed Reading (1983, p. 329) sees no unresolvable conflict between “depth” and the motor theory.

The different methods of detection of ARC are likely to remain ‘a source of controversy. The Bagolini glass and the synoptiscope are, in many workers’ experience (e.g. Mallett, 1967). so much more sensitive than the more traditional synoptophore and after-image methods that any attempt to demonstrate or disprove instrumental hierarchies must include these more recent devices and use unselected strabismic subjects. All the methods have the disadvantage of being completely subjective. Objective data on the existence of ARC in humans would be very welcome. The present visually evoked cortical potential data (Campos, 1980) are at best rather tentative.

To fit our present knowledge of ARC into any coherent pattern which both accounts for

366 J . A. M. Jennings

harmonious and unharmonious ARC and en- compasses the adaptive and motor theories is a daunting task.

Unharmonious ARC is an extremely unusual find- ing with the Bagolini glass, Bagolini (1967), and Mallet (1970b, 1979) proposes that if it is found under such circumstances, it is caused by a change in the habitual deviation of a subject who for some reason cannot co-vary his previously harmonious ARC.

The adaptive theory fits in well with clinical observation in small-angle and microstrabismic patients. The fixity of the ARC in these constant squints and the quality of stereopsis make a genuinely adaptive mechanism plausible. This could be similar to the adaptation demonstrated electro- physiologically by Shlaer (1971) and Shinkman and Bruce (1977), i.e. an abnormal facilitation of cortical synapses to produce a change in retinal correspon- dence for small deviations. Whether this supports genuine fusional movements remains to be clearly demonstrated.

However, many squints are not small yet they still have harmonious ARC even though the angle of squint varies from distance to near, or when looking up and down. The Bagolini glass indicates that the subject perceives a continuous binocular panorama but stereopsis is severely limited. A prism placed before the deviating eye frequently produces a com- pensating change in convergence often described as an “anomalous fusional movement”. Its slow time course and lack of precision make a change in tonic convergence a more likely possibility. This leads to two interesting possibilities: either single anomalous binocular vision is maintained by co-variation of the angle of anomaly or an “anomalous fixation disparity” is supported by the large pseudo-Panum’s Areas and then this is slowly relieved by the change in tonic convergence (c.f. Schor, 1980). Experimental distinction between these two mechanisms will require considerable ingenuity. This variable ARC ha5 little in common with adaptive mechanisms and a motor basis seems more appropriate.

I t might be that the more plastic ARC, e.g. type A (Mallett, 1970b), is a “motor” mechanism whereas the more stable ARC, e.g. type C, is an “adaptive” mechanism. Perhaps the mixing of cases of anomalous correspondence which arise from under- lying mechanisms of different aetiology has been a contributory factor in previous controversies. Careful measurement of the quality of stereopsis may prove to be a simple way to classify the ARC as adaptive or motor.

CONCLUSION The intention of this review has been to emphasize

those areas of controversy within ARC which would benefit particularly from further experimental investigation. The development of more objective techniques and the resolution of such issues as the form of the horopter, the quality of stereopsis, “fusional” eye movements and “depth” of ARC, will allow further progress in our understanding of this puzzling phenomenon.

Acknowledgements-I am grateful to Dr W . N. Charman, Professor L. D. Pickwell and the manuscript reviewers for their most helpful advice and suggestions.

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