Sensory and sensori-motor adaptations in strabismus: Their role in space perception

4cta Psychologica 63 (1986) 281-295 North-Holland

281

SENSORY AND SENSOR&MOTOR ADAPTATIONS IN STRABISMUS: THEIR ROLE IN SPACE PERCEPTION

Emilio C. CAMPOS * Umversity of Modenu, Italy

Accepted May 1986

In comitant strabismus many perceptual adaptive processes take place, which involve perception of space. Suppression of the image of the deviated eye and anomalous retinal correspondence (ARC) are the two main antidiplopic mechanisms. ARC may be present without suppression in small-angle strabismus (up to 10 degrees), supporting an anomalous binocular cooperation in spite of the deviation. Both psychophysical and electrophysiological evidence for anomalous binocular vision in strabismus are provided. Sensori-motor adaptations in strabismus develop as well. They are represented by vergence eye movements which, although not identical to, have similar characteristics as normal fusional vergences. These anomalous fusional eye movements tend to return the eyes to their original deviation when elements are introduced to change the position of the eyes, e.g., prisms or surgery. In conjunction with ARC, these movements serve to maintain binocular visual perception despite the strabismus.

Sensory and sensori-motor consequences take place in comitant strabismus, i.e., a strabismus (deviation of one eye) in which the angle of deviation does not vary significantly in different gaze positions. These consequences are a common adaptation of the patient to the angle of deviation. In essence, mechanisms are employed which attempt to provide a perception of space as similar as possible to that of normals, in spite of the deviation of the visual axes.

In any type of strabismus, diplopia and confusion initially take place. Diplopia is that condition for which similar images are perceived by retinal elements with different directional localization (disparate retinal elements). Confusion is the consequence of the two foveae stimulated by different images. In childhood, diplopia and confusion are first eliminated by means of suppression of the image of the

* Author’s address: E.C. Campos, Clinica Oculistica dell’Universit8 di Modena, Via de1 Pozzo 71, 41100 Modena, Italy.

OOOl-6918/86/$3.50 0 1986, Elsevier Science Publishers B.V. (North-Holland)

282 E.C. Campos /Adaptation mechanisms in strabismus

deviated eye. Elimination of diplopia and confusion through suppression is achieved at considerable cost, because all binocular functions are lost. Later on, in some patients, mainly in subjects with small-angle strabismus (no more than 10 degrees of deviation) another anti-di- plopic mechanism develops, namely anomalous retinal correspondence (ARC). ARC provides to a certain extent binocular cooperation.

The aim of this paper is to discuss how ARC serves to support a sort of binocular vision in strabismus which is maintained by vergence movements, tentatively referred to as anomalous fusional movements (a.f.m.).

Anomalous retinal correspondence

ARC can be defined as a functional rearrangement of the spatial ‘value of the retinal elements. According to classical theory, for each retinal element in one eye, there is normally only one retinal element in the fellow eye that corresponds to the same position or direction in space. These are corresponding elements.

The normal spatial correspondence of the retinal images is disrupted in strabismus. Because of ocular deviation, corresponding points in space are projected onto non-corresponding retinal elements. Ordin- arily, this would produce diplopia, an extremely debilitating condition. Fortunately patients with onset of strabismus in childhood do not experience prolonged diplopia. Often the information from one eye is completely suppressed. Clinical research shows, however, that suppression is not always complete. Some patients acquire some binocular integration, as though the spatial ‘map’ of the deviated eye has shifted so that anatomically disparate retinal positions gain functional correspondence with the spatial coordinates of the fellow eye. Thus, the patient may be capable of binocular visual localization and in certain cases even of coarse stereopsis. This adaptive modification of binocular correspondence is referred to as anomalous retinal correspondence (Bagolini 1967).

Sensory and motor fusion

Sensory fusion and motor fusion are two distinct processes which are strictly interconnected and sustain normal binocular vision. Sensor3

E.C. Campos / Adaptation mechanisms in strabismus 283

fusion is the capability of a subject to have single binocular perception. Sensory fusion takes place when sufficiently similar images are projected onto corresponding retinal elements of the two eyes. If dissimilar stimuli are projected, retinal rivalry is obtained and sensory fusion is impossible. On the other hand, if equal stimuli are projected onto disparate retinal elements, diplopia results.

Motor fusion refers to the fusional or vergence eye movements that maintain the retinal images on corresponding retinal elements as fixation distance changes. Fusional movements are stimulated by retinal disparity and should be differentiated from vergence movements that accompany change of ocular accommodation (accommodative vergence). Fusional vergence normally occurs whenever stimuli of sufficiently similar size, structure, luminance and color are projected onto disparate retinal elements. This mechanism is effective, however, only when the disparity of the stimuli is inside the fusional range of the subject. Fusional vergence can therefore be considered to be a sensori- motor phenomenon. The input is sensory (i.e., retinal disparity) and the output is motor (i.e., a vergence movement). Corresponding retinal elements, e.g., typically the two foveae, are said to hold a zero reti- nomotor value, because no movement is necessary to obtain single binocular vision. The motor value, which specifies the vergence movement required for fixation, increases with increasing retinal disparity (Von Noorden 1985).

Fusional vergence is most effective in convergence. However, it exists to a lesser extent in divergence as well as in verticality.

Clinically, motor fusion is normally tested with prisms or with the major amblyoscope (synoptophore). This latter instrument is a haplo- scope made up of two arms which can be moved. The change in position is expressed in degrees. Each arm houses a slide on which different stimuli are reproduced and projected to one eye only. Thus, fusional movements can be easily stimulated by moving its arms to disparate retinal elements.

A bar of prisms of increasing power in front of one eye can also be used for testing motor fusion. For the analysis of convergence movement, the bar is put so as to have the prisms base-out. Upon interposi- tion of the prism, there is immediately a saccadic movement of both eyes in the direction opposite to that of the base of the prism. If the power of the prism is such as to shift the image of one eye to a disparate retinal element whose eccentricity is inside the fusional range

284 E.C. Campos / Adaptation mechanisms in strabismus

of a given subject, a convergent movement follows thereafter. This is an expression of motor fusion. These vergence movements typically occur within a few seconds (Stark et al. 1982) and under normal conditions it is possible to observe the convergence movement with the naked eye.

Similar observations are obtained for divergence (stimulated by base-in prisms) and vertical vergences (stimulated by base-up and down prisms).

Anomalous binocular vision

Sensory adaptation

It has been demonstrated that in small-angle strabismus (up to 10 degrees of deviation) a binocular cooperation supported by ARC exists. In this situation, there is usually no suppression of the image of the deviated eye.

Using a conveniently modified horopter apparatus, Bagolini (1967) showed that in these patients an area of single binocular vision can be found, which is similar to the Panum’s area of normals and was therefore defined as pseudo-Panum’s area. However, the pseudo- Panum’s area has certain characteristics that clearly differ from the Panum’s area of normals. First, the pseudo-Panum’s area is much wider than the normal Panum’s area, and it is variable in size in the same subject (fig. 1). Whereas the Panum’s area of normals supports stereo- scopic perception, the latter is often absent or coarse, if present, in strabismus (Schor et al. 1983).

The pseudo-Panum’s area can be explained in terms of retinal correspondence (Bagolini 1967). Unlike normals, in patients with ARC one point of the fixing eye corresponds to a more extended retinal area of the deviated eye. Consider, for example, the situation depicted in fig. 2. A patient is looking at a fixation target and the test-stimulus is moved back and forth along the median (or sagittal) plane from A to B. The image of this stimulus moves between a and b on the retina of the deviated eye, but during this movement binocular single perception is maintained. Interestingly, this never occurs in normals thus showing that ARC is much looser and less precise than normal retinal correspondence. I shall analyze later the significance and the aim of the point-to-area correspondence in strabismus.

E.C. Campos / Adaptation mechanisms in strabismus

RE

ORTHOPHORIA

285

SMALL ANGLE STRABISMUS B

Fig. 1. A: For a normal subject fixating a point in space a plane can be defined on which any object point will project images onto corresponding retinal elements (horopter). There is a narrow area in front of and behind the horopter (i.e., Panum’s area) where objects appear single although they are imaged onto slightly disparate retinal elements. Binocular single perception with stereopsis is so achieved. B: In strabismus with Anomalous Retinal Correspondence (ARC) a spatial zone can be found which is similar to but larger than the Panum’s area of normals. This enlarged area of binocular single vision in strabismus is defined pseudo-Panurns’s area.

Anomalous binocular vision can also be demonstrated with tech- niques of binocular campimetry (Campos 1982). Examination of the binocular visual field of strabismics with ARC was performed by having the patient fixate at the center of a tangent screen positioned 1 meter in front of him, with a pair of Bagolini striated glasses in front of his/her eyes. The test-target was a white light source (0.3 degrees diameter) which was moved perimetrically. The patient had to indicate whether he saw one light crossed by two streaks (superimposition of the images of the two eyes), one light crossed by one streak (suppression) or two lights each crossed by one streak (diplopia). With this technique the stimulus was fusable (i.e., equal for the two eyes). If dissimilar stimuli were used retinal rivalry would have been provoked. In patients with strabismus, retinal rivalry inevitably causes suppression of one image.


LE RE

Fovea Fovea eccentric fixinq point

I _

in binocular vision A area of potential anomalous

B correspondence with the fovea / of LE (fixing eye)

1’ I >’ ;

I’ I

pseudo Panum’s area p,” I

‘LE

Fovea Fovea B

Fig. 2. Pseudo-Panum’s area explained in terms of ARC. If a stimulus is moved from A to B its image moves in the deviated eye from a to 6. Still a binocular single perception is maintained. This is due to the fovea of the fixing eye corresponding to a more extended eccentric area of the deviated eye. When the image of the stimulus is moved inside this area there is not necessarily spatial ‘gain’, or there may be just coarse-spatial ‘gain’.

The striated glasses served to differentiate a single perception due to suppression from one attributable to superimposition of the images of the two eyes. They were therefore control-markers for binocularity.

With the above described technique it has been possible to demon- strate the presence of an anomalous superimposition of the two visual fields of more than fifty patients with small angle strabismus and ARC (fig. 3). Inside the examined area which involved roughly 30 degrees of the central field, there was a binocular single perception sustained by ARC with little or no suppression, using the technique employed by us.

Thus, in strabismus, ARC can serve to sustain an anomalous type of binocular perception, by virtue of change from normal retinal correspondence, that allows sensory fusion of anatomically disparate retinal areas.

E.C. Campos /Adaptation mechanisms in strabismus 287

6~ RIGHT ESOTROPIA SG A.R.C. DIPLOPIA WITH BAGOLINI’S RED FILTER No 12

O.D.: S.G. m A.R.C. 0,s.: S.G.

STIMULUS: $0.3’ 115’cd/m’ - BACKGROUND: 5 cd/m’

Fig. 3. Binocular visual field of a patient with a right small-angle esotropia (6”) and ARC as tested with the striated glasses (S.G.). The patient was examined having one striated glass in front of the right eye (OD) and one in front of the left eye (OS). There is an anomalous superimposition of the visual fields of the two eyes. This superimposition is sustained by ARC and makes anomalous binocular vision possible. The projection of the fovea of the left fixing eye (Fos) and that one of the right deviated eye (F,,) are indicated in the central part of the field.

Recent electrophysiological evidence indicates that these psychophysical findings are an expression of binocular cortical integration (Campos and Chiesi 1983). Monocular and binocular visual evoked responses (VER) were recorded in strabismics, whose binocular sensory status was tested with the striated glasses: they showed ARC and suppression. Normals served as control (Campos and Chiesi 1983, 1984).

Both in normals and in strabismics with ARC the binocular VER had a significantly greater amplitude than one in a monocular condition. An example can be seen in fig. 4. Strabismics with suppression never showed a binocular VER whose amplitude was greater than the monocular one. This was also independent from the angle of deviation (fig. 5). It is likely that the enhancement of the binocular VER which

288 E.C. Campos / Adaptation mechanism in strabismus

Q I4 4’ LEFT ESOTROPIA

S.G.: A.R.C.

OD

STIMULUS: 1.46 c/g-7Hz

Fig. 4. The binocular Visual Evoked Response (OU) of a patient with strabismus and ARC is definitely larger than the monocular responses of the right (OD) and left eye (OS). This is defined as summation. A binocular cortical integration is demonstrated objectively. c/g = cycles/degree.

takes place both in normals and in strabismics with ARC is an expression of binocular cortical interaction.

Enhancement of the VER has been defined by us as summation, i.e., an activation of a population of binocular cortical cells. In fact, summation is absent not only in the case of suppression but also in the presence of diplopia (both spontaneous and artificial) (Campos and Chiesi 1983, 1984). If the enhancement was simply attributable to the combined activity of two populations of monocular cells, then it should be present also with diplopia. In our experiments this was never the case. Therefore, our data support the hypothesis that summation is an objective correlate to sensory fusion, because it disappears when fusion is interrupted (diplopia) or absent (suppression).

Sensori-motor adaptations

As noted earlier, normal binocular vision involves motor as well as sensory fusion. In strabismics, the sensory aspect of binocular vision is


6 23 25O LEFT ESOTROPIA S.G.: SUPPRESSION OS

Q 16

8” LEFT ESOTROPIA S.G.: SUPPRESSION OS

v&J- 4vv; L 20 msec STIMULUS: 1.46 c/g-7Hz

Fig. 5. In case of strabismus with suppression, Visual Evoked Responses summation is absent, independent from the amount of the angle of deviation. OD: right eye; OS: left eye; OU: binocular response; S.G.: striated glasses; c/g: cycles/degree.

sustained by ARC and the motor aspect by vergence movements. Vergence movements occur whenever a change in the angle of strabismus is spontaneously or artificially induced, and can be analyzed particularly well by means of prisms.

Prisms have been used widely for both diagnostic and therapeutic purposes in strabismus. Attempts have been made to favor a re-align-

290 E.C. Campos /Adaptation mechanisms in strabismus

ment of the eyes through bifoveal stimulation. Consider, for example, convergent ‘strabismus, i.e., esotropia, for which base-out prisms can be used to shift the images so that they are projected on the two foveae. In this way, the strabismus is eliminated optically.

However, often after a few minutes or even some hours, the prismatic ‘correction’ has been partially or totally compensated by the patient, who in orthoptic jargon’is said to have ‘eaten-up’ the prisms and shows strabismus again. Thus, a change in the position of the eyes behind the prisms have been achieved through vergence movements which are too slow to be seen with simple observation. Clinical research indicates that the compensation of base-out prisms commonly takes place in patients with small-angle esotropia and ARC (Bagolini 1976). Moreover, similar compensation has also been found to occur for base-in and base-up/down prisms, in the same type of patients, i.e., with small-angle esotropia (Campos and Zanasi 1978). Finally, vergence movements were also observed in patients with esotropia and ARC at the major amblyoscope (Campos and Catellani 1978). Here, the arms of the instrument were stabilized so that the two foveae could be stimulated. The amount of the displacement of the arms of the synoptophore was an expression of the angle of deviation. The patients were asked to fixate at targets positioned in the arms of the synoptophore and imaged at infinity. Various types of stimuli were used. It was noted that after some minutes of observation, the stimuli were no longer projected on the two foveae. A further shift of the arms of the instrument was necessary in order to reestablish the initial situation. This phenomenon is in essence superimposable to the ‘eating-up’ of prisms. In fact, a change in the deviation occurred as well. Note that proximal convergence, ordinarily present, has different features when examining a subject at the synoptophore. It is instantaneous both in normals and strabismics.

The compensation for prisms is essentially an attempt by the patient to ‘realign’ the motor system to his/her binocular sensory adaptation by means of vergence movements. This happens whenever prisms are used either to decrease or increase the deviation. Because of the similarity of this phenomenon with fusional vergences, it has been tentatively defined as anomalous fusional movements (a.f.m.).

Horror fusions and diplopia-phobia are two conditions which were considered to be the cause of spontaneous increase of the angle of strabismus. Some patients were thought to be unable to fuse and had


therefore their eyes misaligned, whatever treatment was instituted (horror fusions.). Other patients were thought to increase their deviation in an attempt to displace the image of the deviated eye in order to avoid diplopia (diplopia-phobia). Both conditions lack a convincing demonstration. In essence they may be considered as an expression of a.f.m. (Campos and Zanasi 1978).

A.f.m. have the aim of bringing relatively similar images onto retinal areas which correspond in an anomalous way. A.f.m., however, have been shown to be effective, although with a considerable increased time course, even when non-fusable stimuli were projected to the two eyes with the major amblyoscope (Campos and Catellani 1978) and occasionally in the presence of suppression associated with ARC in the periphery of the visual field (Bagolini 1976). Therefore, a.f.m. appear not to be as strictly interconnected with A.R.C. as normal fusional movements are with normal retinal correspondence. It has been pos- tulated that a.f.m. are effective in strabismus when a change in the retino-motor value of retinal elements takes place, as happens for the directional localization in A.R.C.

The zero retino-motor value is held, e.g., by the fovea of the fixing eye and an eccentric area of the deviated eye and not by the two foveae (Bagolini 1976; Campos and Zanasi 1978). Thus, whenever a displacement of an image takes place, from retinal elements which have acquired a zero retino-motor value, vergence movements take place.

Another interpretation for a.f.m. can be sought in the slow fusional vergence system also present in normals. Schor (1983), on the basis of Ogle and Prangen’s work (1953), suggests that there is a fast and a slow mechanism for fusional vergences. The stimulus for fast fusional vergences is retinal image disparity. Slow fusional vergence appears to be stimulated by the effort (output) of the fast fusional vergence control mechanisms. It is thought to determine the resting or ‘tonic’ vergence posture when there is no disparity stimulus. Several investigators have proposed that this slow or tonic vergence may play an important role in vergence adaptation (e.g., Carter 1965; Ebenholtz 1981; Owens and Leibowitz 1980, 1983).

A.f.m. could therefore be considered to be an expression of the slow mechanism, which is the only one left in strabismus. Obviously, further studies are necessary to attempt to clarify this interesting point. In fact, the question remains of how slow fusion can exist in the absence of a noticeable fast fusion. The characteristics of the sluggish vergence

292 E.C. Ccrmpos / Aduptution mechanisms in strabismus

movements sometimes observed in strabismics as an expression of fast vergence need to be analyzed in depth.

A.f.m are slow, sometimes not precise, and can be of different strength. This means that they may be able to only partially fulfill their action of compensating for prismatic correction. The imprecision of a.f.m. may also be due to ARC being a much looser mechanism than N.R.C. In any event, both in m.f.m. and a.f.m. there is an increase of the tonus of the medial recti when base-out prisms are anteposed to the eyes. Both m.f.m. and a.f.m. are most effective in convergence but also exist in divergence and verticality, i.e., they are able to compensate for higher prismatic applications in convergence than in other directions.

The aim of a.f.m. is to maintain the angle of deviation in which anomalous binocular vision is effective. They are therefore a major handicap for surgery, because they tend to reduce the effect of a correctly planned procedure. A.f.m. are thus thought to be responsible for restoring the patient’s original deviation (Bagolini 1984). This is probably due to the binocular comfort of the patient being best adapted to the pre-operative angle of strabismus (Bagolini and Campos (1982). The supposed shift in the retino-motor value can explain this effort of the patient’s restoration of the original deviation.

That fusional movements exist in strabismus in association with ARC was first reported by Hallden (1952), who did not specify, however, whether they were normal or anomalous. Ophthalmologists often speak of ‘peripheral fusion’ and admit its existence in strabismus, implying however that it is normal. Central fusion is denied in strabismus. The concept of central versus peripheral motor fusion is strongly related to the major amblyoscope. When the stimuli depicted in the targets involve the central field, central fusion is claimed to be tested. Large stimuli are used to investigate peripheral fusion.

The presence of normal peripheral fusion in strabismus is nevertheless unlikely. In fact, in order to have a normal motor fusion mechanism, retinal correspondence has to be normal as well. I have demonstrated however that if ARC develops, it involves the whole visual field (Campos 1982). Therefore, ARC also exists in the periphery. It would therefore be difficult to understand how normal motor fusion could be connected with ARC. The peripheral fusion is presumably made up by a.f.m. On the other hand, it has been stated by Stark et al. (1982) that no disparity vergence movements exist in strabismus. According to Stark et al. there is a ‘saccadic substitution’ instead. This statement is

E.C. Cumpos / Adaptation mechanisms in strabismus 293

made on the basis of accurate recordings, whose time course was nevertheless inappropriate for strabismus. In fact, fusional vergence movements are very slow, whereas Stark et al.‘s recordings did not last more than a few seconds. Preliminary experiments underway in my laboratory show the existence of vergence in strabismus when the recording is extended to several minutes. Fast vergence movements are occasionally present in some patients but are difficult to investigate because of their reduced amplitude. Probably, if indeed a.f.m. can be an expression of a normal or partially altered slow fusion mechanism, then Stark et al.‘s results are not surprising.

Another point which has to be stressed is that the patients tested in my laboratory have been carefully evaluated from the binocular sensory standpoint with Bagolini’s striated glasses. This allows us to state that a.f.m. are present mainly in strabismus with ARC. Patients with strabismus with large angle of deviation usually show suppression of the image of one eye. They do not exhibit a.f.m. Stark et al. did not provide sufficient information on the binocular sensory status of their subjects, in that they did not specify the testing procedure used to establish the presence of ARC, etc. (It is known that the testing procedure strongly influences results of a binocular sensory status analysis).

Furthermore, the hypothesis by Stark et al. (1982) that vergence movements in strabismus are induced by accommodative vergence rather than by disparity is probably incorrect. It must be stressed that all the observations by Bagolini and myself, both together and indepen- dently, were made on patients wearing their full retinoscopic correction. If an angle of strabismus is measured for distance under these circumstances, accommodation plays no role in possible variation of the deviation. If the resting point for accommodation does not coincide with infinity in all patients, one could argue that variations in the angle of deviation are to be attributed to an active relaxation of accommodation. However, this is not the case for the patients tested by us for two reasons. First, they showed convergence movements whereas relaxation of accommodation would induce divergence movemens. Second, patients had an optical correction based on cycloplegic retinoscopy. As, a consequence, for distance, accommodation could not play a role in changes of the angle of deviation.


Concluding remarks

In conclusion, it would be interesting for non-ophthalmologists to be aware of the adaptational mechanisms which take place in comitant strabismus. They are all aimed to maintain a space perception as similar as possible to that of normals, in spite of the deviation. Sensory adaptation allows a binocular anomalous cortical integration. Sensori- motor adaptations keep stable the deviation in which binocular integration is useful for the patient. The old concept of strabismic patients being regarded as functionally monocular, has to be changed. Clearly, the degree of binocularity of these patients is not as sophisticated as that of normals. Nevertheless, the only function which is significantly reduced or even absent is stereopsis, whose practical importance may be questioned.

References

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Bagolini, B. and E.C. Campos, 1982. ‘Disjunctive movements in comitant strabismus’. In: G. Lennerstrand et al. (eds.), Functional basis of ocular motility disorders. Wenner-Gren Sym- posium Series 37,109-111.

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Carter, D.B., 1965. Fixation disparity and heterophoria following prolonged wearing of prisms. American Journal of Optometry and Physiological Optics 42, 141-152.

Ebenholtz, SM., 1981. ‘Hysteresis effects in the vergence control system: perceptual implications’. In: D.E. Fisher, R.A. Monty and J.W. Senders (eds.), Eye movements: visual perception and cognition. Hillsdale, NJ: Erlbaum.

Hallden, U., 1952. Fusional phenomena in anomalous correspondence. Acta Ophthalmologica Suppl. (Copenhagen) 37, l-93.

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Ogle, K.N. and A. Prangen, 1953. Observations of vertical divergences and hyperphorias. Archives of Ophthalmology 49, 313-334.

Owens, D.A. and H.W. Leibowitz, 1980. Accommodation, convergence, and distance perception in low illumination. American Journal of Optometry and Physiological Optics 57, 540-550.

Owens, D.A. and H.W. Leibowitz, 1983. ‘Perceptual and motor consequences of tonic vergence’. In: CM. Schor and K.J. Ciuffreda (eds.), Vergence eye movements: basic and clirrcal aspects. Boston, MA: Butterworth. pp. 25-74.

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Schor, CM., B. Bridgeman and C.W. Tyler, 1983. Spatial characteristics of static and dynamic stereoacuity in strabismus. Investigative Ophthalmology & Visual Science 24, 1572-1579.

Stark, L.W., K.J. Ciuffreda and R.V. Kenyon, 1982. ‘Abnormal eye movements in strabismus and amblyopia’. In: G. Lennerstrand et al. (eds.); Functional basis of ocular motility disorders. Wenner-Gren Symposium Series 37, 71-82.

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Sensory and sensori-motor adaptations in strabismus: Their role in space perception