Binocular Sensory Changes in Strabismus
Diplopia and Confusion
Diplopia occurs when a patient sees two images of one object. Fig. 12.1 A represents an adult with recent onset left esotropia. The patient is viewing an isolated letter ‘A’, with no other objects present in the field of view. The letter is imaged on the right fovea (f) but, because the left eye is convergent, it is imaged on a nasal region of the left retina (p) which is not the fovea. In other words, the object is imaged on noncorresponding retinal points. Therefore, the object is perceived in two different visual directions, causing diplopia.
Everyday visual scenes are usually more complicated than the single object in Fig. 12.1A . Fig. 12.1B illustrates the situation, for the same patient, when there are two isolated objects in the visual field (of course, this is still an unrealistically straightforward example). The letter A is imaged on the fovea of the right eye and the letter B is imaged on the fovea of the left eye. As the case is a recent onset strabismus in an adult patient, the patient is likely to have normal retinal correspondence (NRC). This means that both foveae share the same visual direction, so the patient will see the two letters as being superimposed. The visual perception is described as confusion . Of course, the diplopia illustrated in Fig. 12.1A would also be present in the situation illustrated in Fig. 12.1B , so in everyday scenes, both diplopia and confusion will coexist. Depending on the visual scene and the magnitude of the separation of the images, diplopia may be more troublesome than confusion.
Suppression of the Binocular Field of the Strabismic Eye
Clearly, diplopia and confusion are undesirable, so the visual system may develop sensory adaptations to avoid them. In young patients, this is what happens. Hypothetically, one method of avoiding symptoms in strabismus might be to suppress the whole of the binocular field of the strabismic eye. This sometimes occurs ( Joosse et al., 2005 ), particularly in divergent strabismus ( Ansons & Spencer, 2001 ), and in decompensated exophoria, suppression is more likely in cases exhibiting intermittent exotropia ( Wakayama et al., 2013 ). The investigation and treatment of suppression is detailed in Chapter 14 . However, the visual system usually does not adopt such wasteful measures. Instead of having a large area of suppression, a strabismic patient who is young enough to have a reasonable degree of sensory plasticity usually will develop harmonious anomalous retinal correspondence (HARC). Suppression and HARC are fundamentally different, and elicit different steady state visual evoked potentials ( Bagolini, Falsini, Cermola, & Porciatti, 1994 ).
Anomalous (Abnormal) Retinal Correspondence (ARC)
The classical views on Panum’s fusional areas and retinal correspondence have, as a result of research over the last 20 years, undergone much revision. The phrase ‘corresponding retinal points’ is something of a misnomer: a point image on one retina actually corresponds with point images falling in a Panum’s area in the other eye. Several researchers have shown that Panum’s area is not a fixated entity, but its size varies according to the parameters of the target. What remains unclear is whether, at a given retinal eccentricity, the size of Panum’s area really changes or whether apparent changes are experimental artefacts.
Several studies have obtained data indicating that retinal correspondence can change in normal, nonstrabismic, observers ( Fender & Julesz, 1967 ; Hyson, Julesz, & Fender, 1983 ; Erkelens & Collewijn, 1985 ; Brautaset & Jennings, 2006a ; Fogt & Jones, 1998 ), or that Panum’s fusional areas are much larger than previously believed ( Collewijn, Steinman, Erkelens, & Regan, 1991 ). However, one very thorough paper has concluded from two experiments that retinal correspondence is fixed in nonstrabismic observers ( Hillis & Banks, 2001 ).
There is certainly the need for some flexibility in the vergence system as, during everyday vision and head movements, small errors in vergence occur. This is particularly likely after a large saccade and represents a small breakdown in Hering’s law. This is probably why our visual system has evolved to have Panum’s fusional areas rather than inflexible point to point correspondence.
Anomalous Retinal Correspondence in Strabismus
Panum’s fusional areas mean that, in nonstrabismic people, NRC can tolerate small vergence errors, without losing fusion or stereopsis. This impressive feat of cortical processing is far surpassed by the ability of children, who are young enough to possess considerable neural plasticity, to exhibit large shifts in retinal correspondence to compensate for strabismus. The purpose of this anomalous retinal correspondence (ARC) is for a point on the retina of the good eye to correspond with a new point in the retina of the strabismic eye that differs from its natural, innate, corresponding retinal point. Clearly, the newly corresponding points should be set at the angle of strabismus. This is nearly always the case in ARC and there is said to be harmonious anomalous retinal correspondence (HARC; Evans, 2001d ). The angle through which the retinal correspondence has been shifted from the normal is called the angle of anomaly . The term ‘anomalous retinal correspondence’ has been criticised because the anomalous correspondence occurs cortically, not on the retinae. Despite this semantic objection, it is often easier to conceptualise the effect of HARC by considering retinae, so the convention will be followed here.
In HARC, the patient has no diplopia and so the subjective angle of deviation is zero. The cover test usually shows a strabismus which can be estimated or measured (p. 20) to be the objective angle of deviation . The difference between the objective angle and subjective angle is the angle of anomaly.
Research in nonstrabismic subjects to investigate the largest amount of visual disparity that can still provide depth information may help to understand the basis for HARC ( Dengler & Kommerell, 1993 ). All the subjects who were tested could recognise disparities of up to 6 degrees, and one up to 21 degrees, without making compensatory vergence eye movements. It is possible that far-reaching interocular cortical connections in normal subjects might also be utilised in cases of strabismus ( Dengler & Kommerell, 1993 ), although it should be noted that HARC is uncommon in vertical strabismus (von Noorden, 1996 ).
The precise mechanism of HARC remains unclear. One view is that remapping of Panum’s areas occurs ( Lie, Watten, & Fostervold, 2000 ). Another view is that Panum’s areas become enlarged, although this has been disputed ( Helveston & von Noorden, 1967 ). A third hypothesis is that in HARC the bifoveal assumption is abandoned, and the position of each eye is registered separately, probably on the basis of muscle activity ( Jennings, 1985 ). This form of HARC would be most likely to facilitate the perception of direction, not depth and distance. It might account for HARC in large angle strabismus, with the ‘cortical remapping hypothesis’ accounting for HARC in cases of small-angle strabismus (Jennings, personal communication).
To summarise, there are three types of binocular sensory status in strabismus. First, there may be no adaptation, resulting in diplopia and confusion. Second, all the binocular field of the strabismic eye may be suppressed. Third, HARC may occur. The third option allows some rudimentary form of ‘pseudobinocular vision’ and is clearly the preferable outcome, so the question arises, why does this not always occur? This, and some limitations and consequences of ARC, will now be considered.
Factors Influencing the Development of HARC
Although the precise neurophysiological basis of HARC is not known, the main theories all accept that this ‘stunning feat of cortical processing’ ( Nelson, 1988b ) must, inevitably, have limitations. One of these limitations relates to the requirement for the visual system to be plastic for HARC to develop. It is therefore not surprising that a younger age of onset of strabismus is associated with a greater likelihood of HARC being present. Von Noorden (1996) states that HARC, albeit superficial (see later), can develop as late as the early teenage years. A survey of 195 patients by Stidwill (1998) found that 97% of cases of HARC had developed in strabismus with an onset before the age of 6 years, although the condition was occasionally present in strabismus developing up to the age of 15 years.
In cases of intermittent strabismus, the visual axes will sometimes be straight, and the patient will have NRC; yet at other times there will be a strabismus and the patient will have HARC. The change from NRC to HARC can be sudden or gradual. The term covariation describes the angle of anomaly covarying with the objective angle of strabismus. Covariation is likely to place additional neural demands on the visual system and hence constant strabismus will be more likely to develop HARC than intermittent or variable strabismus. For similar reasons, unilateral strabismus is more likely to develop HARC than alternating strabismus.
Von Noorden (1996) stated that the rate of occurrence of HARC ‘is high in infantile esotropia, less common in exotropia, and uncommon in vertical strabismus’. Other authors have noted that suppression is more common in exotropia and in anisometropia.
Photoreceptor types, receptive field sizes, and ganglion cell types, vary across the retina. An area of retina near the fovea of 1 mm 2 has a much greater cortical representation than 1 mm 2 of retina in the periphery: this has been termed cortical magnification . The cortical processing task of remapping anomalously corresponding points must be easier if these points are at similar eccentricities from the fovea. Hence, small angle strabismus is more likely to develop HARC than large angle strabismus ( Wong, Lueder, Burkhalter, & Tychsen, 2000 ).
Depth of HARC
Most patients who exhibit HARC can, under certain circumstances, be made to exhibit NRC. In other words, the neural substrate for innate NRC is still present. The difficulty in eliciting NRC is termed the ‘depth of anomaly’ ( Nelson, 1988b ). The factors that make it easier for the visual system to develop HARC are also likely to make the HARC deeper. Therefore, it follows from the previous section that patients are more likely to have deeper (c.f., shallow) HARC in cases where there is a younger onset ( Kora, Awaya, & Sato, 1997 ), a stable angle of strabismus, unilateral strabismus, and a small angle.
The Detection and Treatment of HARC
HARC can be thought of as ‘pseudobinocular vision’. It was noted in Chapter 2 that a patient with weak normal binocular vision (e.g., a decompensating heterophoria) could, by using tests which tend to dissociate the eyes, be ‘broken down’ so the heterophoria degenerates into a strabismus. An analogous phenomenon can occur with shallow HARC. If a patient with shallow HARC is tested with unnatural stimuli, such as after-images or the synoptophore, the pseudobinocular vision may be broken down into NRC, with resulting diplopia or compensatory suppression. If more natural, ‘associating’, tests are used, such as Bagolini lenses ( Chapter 14 ), HARC may be detected. This is why, if the practitioner is to discover whether HARC is truly present under normal everyday viewing conditions, naturalistic tests should be used. The factors which are particularly important in simulating normal visual conditions are listed in Chapter 14 .
The likelihood of treatment succeeding is influenced by the depth of HARC and the age at which treatment is commenced. The shorter the interval between the age of onset of HARC and age at commencement of treatment, the better the prognosis. This highlights the importance of regular professional eyecare for pre-school children, especially if the child is at risk of strabismus.
Sensory Function and Localised Suppression in HARC
In HARC, a point in the peripheral retina of the strabismic eye is said to acquire, during everyday binocular viewing, the same visual direction as the fovea of the fixating eye: this point is directed towards the object of regard and is sometimes referred to as the zero point , zero point measure, or diplopia point ( Serrano-Pedraza, Clarke, & Read, 2011 ). The zero point has also been referred to as the pseudofovea, but this can be confusing because ‘pseudofovea’ is also used to describe the eccentrically fixating area in eccentric fixation. When the good eye is occluded, the patient fixates with the eccentrically fixating point or, if there is no eccentric fixation, with the fovea and this why the cover test works (for an exception, see Chapter 16 ).
The issue of the exceptionally small receptive field sizes at the fovea was mentioned earlier and this makes HARC difficult in two regions of the strabismic visual field. These areas are the fovea and the zero point. If HARC is not possible in these two areas, the alternative is suppression, and suppression at these two areas is a very common finding in the strabismic eye. These small suppression areas that occur in the presence of HARC are quite different to the complete suppression of the binocular field of the strabismic eye that occurs as an alternative to HARC ( Serrano-Pedraza et al., 2011 ). The central suppression areas in HARC are of the order of 1 degree ( Mallett, 1988a ) and often cause, in the Bagolini lens test, the central part of the streak to be absent ( Chapter 14 ). The central suppression areas are also why the modified (large) OXO test should be used instead of the smaller OXO test to assess HARC ( Chapter 14 ). The cortical task of ‘remapping’ will be increasingly difficult as the angle of the strabismus increases, because larger peripheral receptive fields will have to be ‘remapped’ to anomalously correspond with smaller central receptive fields in the other eye. Therefore, if all other factors are constant, it seems likely that with larger angles of strabismus the suppression areas will be larger and pseudostereopsis and pseudomotor fusion (see later) will generally be worse.
The purpose of HARC is to compensate for the strabismus: to provide ‘pseudobinocular vision’. Some pseudostereoacuity is possible with HARC ( Mallett, 1977 ). This is more likely to be present and to be better with deeply-ingrained HARC, particularly with small angled strabismus ( Henson & Williams, 1980 ). Stereoacuity can be better than 100ʺ with the Howard-Dolman or Titmus circles tests ( Jennings, 1985 ) which measure contoured stereopsis, but it has been argued that random dot stereopsis cannot be demonstrated in a patient with strabismus ( Cooper & Feldman, 1978 ; Hatch & Laudon, 1993 ). Rutstein and Eskridge (1984) argued that some patients with small-angle strabismus have demonstrable stereopsis with random dot tests which is indicative of normal correspondence. Yet another view is that stereopsis is not possible in any form of constant strabismus, even microtropia, and findings to the contrary are attributable to monocular cues in stereotests ( Cooper, 1979 ).
The locus of the horopter and anomalous fusional space in HARC is much larger than in normal binocular vision ( Jennings, 1985 ). A great many questions remain unanswered about the physiological basis for the antidiplopic strategies of suppression and HARC ( Serrano-Pedraza et al., 2011 ).
Motor Function in HARC
In cases of NRC the objective angle will equal the subjective angle. In HARC, the patient will have single vision, so their subjective angle is zero. The angle of anomaly is equal to the difference between the subjective and objective angles. So, in HARC the angle of anomaly is equal to the objective angle: the HARC fully corrects the subjective angle of strabismus.
The objective angle normally exhibited by the patient under undisturbed conditions is called the habitual angle of strabismus , and the objective angle following prolonged or repeated dissociation is the total angle of strabismus . As the habitual angle changes to the total angle, the angle of anomaly usually remains constant: the difference between the new total objective and subjective angles is the same as that between the habitual objective and subjective angles ( Table 12.1 , first 3 columns). The fact that the total angle is reduced to the habitual angle during everyday viewing implies that the HARC may induce some motor fusion to maintain the habitual angle. Indeed, vergence movements can occur in HARC and the patient can be seen to ‘converge’ to follow an approaching target, yet a cover test will reveal that the strabismus is present. Similarly, ‘pseudo’ fusional reserves can often be measured.
