6

Sensory Aspects of Kenneth W. Wright

SENSORY ADAPTATIONS

Visual neurodevelopment changes in response to abnormal stimulation from a blurred retinal image or strabismus. These changes are referred to as sensory adaptations. The specific type of sensory adaptation depends on when the abnormal visual stimulation occurred, the severity of the abnormal stimulation, and type of binocular disruption. In Chapter 4, we discussed cor- tical and , which are basic sensory adap- tations to a blurred image or strabismus. This chapter provides a list of more specific sensory adaptations that are encountered clinically. These adaptations are divided into two sections based on the onset of the sensory insult: (1) visually mature and (2) visually immature. A discussion of important sensory tests is provided at the end of this chapter.

MATURE

The following sensory adaptations occur after the development of bifoveal fusion, when the visual system is mature. Visual development continues until approximately 7 to 8 years of age. After that, there is minimal visual-neurological plasticity. There are some exceptions, however, and prolonged visual plasticity into adulthood has been reported (see discussion at the end of this section: Prolonged Visual Plasticity).

Diplopia Acquired strabismus in patients over 7 or 8 years of age usually results in double vision (i.e., ). Diplopia is also reported

174 chapter 6: sensory aspects of strabismus 175 in younger children with acquired strabismus, but it is usually transient and lasts only 2 to 4 weeks before the diplopia is cor- tically suppressed. The patient with diplopia will fixate on an object with one fovea, and see a diplopic image of that object that comes from the perifoveal of the deviated eye (Figs. 6-1, 6-2). The fovea of the deviated eye is suppressed to avoid simultaneously seeing two different objects, one from each fovea (see below: Confusion). Thus, the patient with one eye fixing on

Red Filter

Patient's Perception

Uncrossed Diplopia FIGURE 6-1. with uncrossed diplopia. The image of the skier falls on the fovea of the left eye and on the nasal retina of the deviated right eye. A red filter over the right eye causes the diplopic image from the right eye to be red. Note at the bottom of the figure: the patient per- ceives the red image from the right eye to be located to the right of the clear image, resulting in uncrossed diplopia. 176 handbook of pediatric strabismus and amblyopia

Red Filter

Patient's Perception

Crossed Diplopia FIGURE 6-2. with image falling on the fovea of the left eye and on temporal retina of the right eye, causing crossed diplopia. A red filter over the deviated right eye causes the diplopic image from the right eye to be red. Note at the bottom of the figure: the patient perceives the red image from the right eye to be located to the left of the clear image, result- ing in crossed diplopia. a painting and the deviated eye pointed to a lamp will see two paintings, not a painting superimposed on a lamp. The image from the fixing eye will be in clear focus located directly in front of the patient, while the diplopic image from the deviated eye will appear blurred and off center because it comes from the peripheral retina. chapter 6: sensory aspects of strabismus 177

OD fixing RE LE

FIGURE 6-3. Patient with a left . A red filter over the devi- ated left eye causes the diplopic image from the left eye to be red. The X projects to the fovea of the fixing right eye and to the superior retina of the deviated left eye. Because the superior retina views the inferior visual field, the red diplopic image in the left eye is seen below the clear image from the right eye.

Esotropia causes the image to fall on the nasal retina of the esotropic eye, which projects temporally and causes uncrossed diplopia because diplopic image is on the same side as the deviated eye (see Fig. 6-1). Exotropia causes the image to fall temporal to the fovea of the exotropic eye, which projects to the nasal field, producing crossed diplopia (see Fig. 6-2). We can remember the s in esotropia means same side diplopia (uncrossed), and the x in exotropia means a cross for crossed diplopia. In cases of vertical strabismus, the hypertropic eye per- ceives the object as being below the image from the fixing eye (Fig. 6-3). is a difference in image size between eyes and is a cause of diplopia. Aniseikonia is usually caused by ani- sometropia and is treated with spectacles. An acquired retinal image size disparity up to 7% is usually tolerated, but ani- seikonia over 10% may result in diplopia.

Confusion Under rare circumstances, instead of diplopia, patients with acquired strabismus see two different images superimposed on each other, one image from each fovea. If the right eye is looking at a painting and the left eye is pointed at a lamp, the patient with confusion will see the lamp superimposed on the painting. This simultaneous perception from the fixing fovea and the devi- 178 handbook of pediatric strabismus and amblyopia ated fovea is termed confusion. Most patients with acquired strabismus do not experience confusion because they suppress the foveal area of the deviated eye and see the diplopic image from the peripheral retina. Confusion is exceedingly rare; however, this author has reported a patient with tunnel vision secondary to and acquired strabismus who had con- fusion rather than diplopia.10 The peripheral visual field loss associated with the glaucoma probably forced foveal fixation of the deviated eye. It is likely that suppression of the fovea of the deviated eye is dependent on peripheral retinal stimulation by the diplopic image and, therefore, foveal suppression is not pos- sible when the peripheral field is eliminated.

IMMATURE VISUAL SYSTEM

Sensory adaptations occur when the binocularity is disrupted by strabismus or a blurred retinal image during the first few years of life, usually before 6 years of age. The specific type of sensory adaptation depends on many factors, including the size of the strabismus, whether it is intermittent or constant, the age of onset of the strabismus, and the age when the strabismus is cor- rected. Once childhood sensory adaptations are acquired, they are usually present throughout the patient’s life. Cortical sup- pression is a basic mechanism present in virtually all sensory adaptations to strabismus and a unilateral blurred retinal image. Cortical suppression and amblyopia are discussed in Chapter 4. Herein is a discussion of specific patterns of suppression and abnormal . The following discussion of sensory abnormalities presumes that strabismus is the primary event and that the brain devel- ops sensory adaptations in response to the abnormal visual stimulation. In this author’s view, this is probably true for the majority of strabismus cases; however, strabismus can also occur as a secondary consequence of poor binocular fusion. Examples of a primary fusion deficit and secondary strabismus include sensory strabismus (i.e., unilateral congenital ) and central fusion loss associated with closed head trauma. It should be pointed out that some would argue that most types of childhood strabismus are a consequence of congenitally abnor- mal fusion centers within the brain, not motor misalignment degrading binocular fusion. The answer to this controversy— which came first, the strabismus or the sensory fusion abnor- chapter 6: sensory aspects of strabismus 179 mality?—remains unanswered. The fact that one can recover excellent binocular fusion and stereoscopic vision with early and aggressive treatment suggests that, at least in some cases, the sensory abnormality is secondary to the strabismus.

Monofixation Syndrome (Peripheral Fusion) Small-angle strabismus (10 prism diopters, PD) or mild to mod- erate unilateral retinal image blur in young children and infants causes a suppression of the central visual field of the deviated or blurred eye. The small suppression allows for periph- eral fusion (Fig. 6-4). This sensory adaptation, first described by Marshall Parks, is termed the “monofixation syndrome.”3 Sup- pression is localized to within the central 4° to 5° because the central retina has small receptive fields and high spatial resolu- tion potential; therefore, relatively small differences in image clarity or retinal image position are recognized. In the periph- eral fields, however, slight interocular image differences are not detected, as the peripheral retina has large receptive fields and relatively low spatial resolution. Thus, small retinal image dis- crepancies between the eyes are not disruptive in the peripheral fields, and peripheral fusion occurs. The size of the suppression scotoma is directly proportional to the amount of image blur and size of the strabismus. If the interocular image disparity is too great, even peripheral fusion will be disrupted. Thus, strabismus greater than 10 PD or severe unilateral image blur (e.g., unilat- eral dense cataract) will disrupt even peripheral fusion. These patients will lack binocular fusion and will not have the monofixation syndrome. Because patients with the monofixation syndrome have motor fusion, they often have a relatively large underlying phoria in addition to a small tropia, giving rise to the term phoria-tropia syndrome. Patients with monofixation syndrome usually have stereoacuity in the range of 3000 to 70 s arc, and the central suppression scotoma measures between 2° and 5°. The Bagolini striated test is a sensory test that presents a linear streak of light to each eye oriented 90° apart and centered on the fixation light (Fig. 6-5). Patients with normal binocular vision describe a cross through the center of a fixation light (Fig. 6-5A). In contrast, patients with the monofixation syndrome will describe a cross with a gap in the center of the line pre- sented to the deviated eye (Fig. 6-5B). The gap represents a central suppression scotoma of the nonfixing eye. It is impor- 180 handbook of pediatric strabismus and amblyopia

Small Angle Esotropia

Patient's Perception

Suppression A Scotoma

Anisometropic Amblyopia

Suppression B Scotoma FIGURE 6-4A,B. (A) Diagram of monofixation syndrome secondary to a small-angle esotropia. (B) Hypermetropic with amblyopia. In both cases, patient perceives a clear single image, as the suppression scotoma eliminates the discrepancy from the esotropia and blurred image, respectively. Because of the suppression scotoma, the patient sees one clear image. tant to note that as soon as the dominant fixing eye is occluded, the suppression scotoma vanishes and the patient fixes with the fovea (Fig. 6-5C). The suppression scotoma is often referred to as a facultative scotoma, because its presence is dependent upon fixation with the dominant eye. Worth 4-dot testing is another good method to document the monofixation syndrome. Patients with the monofixation syndrome will fuse the near Worth 4-dot chapter 6: sensory aspects of strabismus 181

A

B

C FIGURE 6-5A–C. Monofixation with microtropia and visual perception with Bagolini lenses. (A) Bagolini lenses over right small-angle esotropia and suppression scotoma, right eye. (B) Retinal images from (A). Note the patient’s perception is one continuous line LE, and one line with an inter- ruption in the center RE. (C) Covering the fixing eye (LE) eliminates the suppression scotoma, and the patient sees a single, continuous line from RE. 182 handbook of pediatric strabismus and amblyopia

(subtends 6° or 12 PD), but suppress the nondominant eye for the distance Worth 4-dot (subtends 1.25°) because it falls within the suppression scotoma. Further descriptions of these sensory tests follow later in the chapter. Patients with monofixation syndrome often have ambly- opia. The amblyopia can be mild (1 or 2 Snellen lines difference) or quite severe (20/200). Even patients with 20/200 amblyopia can still maintain the monofixation syndrome with some peripheral fusion and gross . Clinically, the mono- fixation syndrome is frequently encountered in patients with anisometropic amblyopia, unilateral partial cataract, and small-angle strabismus. Parks described a rare condition, primary monofixation syndrome, which he hypothesized was caused by a congenital lack of central fusion.3

Anomalous Retinal Correspondence Normal retinal correspondence (NRC) is the binocular relation- ship in which the true anatomic foveas of each eye are func- tionally linked together in the occipital cortex. Anomalous retinal correspondence, or ARC, is an adaptation to a moderate- angle infantile strabismus that allows the brain to accept parafoveal retinal images from the deviated eye and superim- poses them with images fixing from the fixing eye. The angle of deviation associated with ARC is usually between 15 and 30 PD, too large to allow peripheral fusion or monofixation. Thus, ARC is a binocular sensory adaptation used to eliminate diplopia by accepting the eccentric image location in the deviated eye as the visual center. This adaptation is a cortical reorganization of retinal correspondence and establishes a new functional fovea called the pseudo-fovea that corresponds to the true fovea of the dominant fellow eye (Fig. 6-6A).8 By cortically establishing a pseudo-fovea at the site of the diplopic image in the deviated eye that corresponds with the true fovea of the fixing eye, the retinal images can be superimposed. ARC and the pseudo-fovea are only present under binocular conditions. When the fixing eye is occluded, the patient changes fixation to the true fovea of the previously deviated eye. If the strabismus of a patient with ARC is partially or fully corrected by surgery or a prism, the image will be displaced off the pseudo-fovea onto the retina that is cortically perceived as being noncorresponding. Because the image is displaced off the pseudo-fovea, the patient will see double even if the image falls chapter 6: sensory aspects of strabismus 183

Patient's Perception

A

B FIGURE 6-6A,B. Anomalous retinal correspondence with right esotropia. (A) Left eye fixes with the fovea (F) and right eye fixes with the pseudo- fovea (PF). The PF corresponds with the esotropia and is located on the nasal retina. Patient perceives a single image as the pseudo-fovea (PF) of the right eye corresponds with the true fovea (F) of the left eye. (B) Placing a base-out prism to partially neutralize the esotropia. The patient fixes the left eye and sees double, as the image now falls temporal to the pseudo-fovea (PF). Images temporal to the pseudo-fovea (PF) will project to the opposite visual field and cause diplopia. 184 handbook of pediatric strabismus and amblyopia on the true anatomic fovea. This type of diplopia is called par- adoxical diplopia. Remember that under binocular viewing the pseudo-fovea is the central orientation of the eye and images dis- placed off the pseudo-fovea will be perceived as falling on non- corresponding retina. Figure 6-6A shows a patient with 20 PD esotropia and ARC with a nasal pseudo-fovea, right eye. Note that after partial correction of the esotropia with a 15 PD base- out prism, the image is now temporal to the pseudo-fovea (Fig. 6-6B). This patient will have crossed diplopia because the image falls on retina that is temporal to the pseudo-fovea, and tempo- ral retina projects to the opposite hemifield. The patient will experience the crossed diplopia so long as the image is tempo- ral to the pseudo-fovea, even if the eyes are aligned so the image falls directly on the true fovea. Adult patients with ARC will often experience some diplopia after correction of their strabismus. An easy way to predict if a strabismic patient has ARC and will have postoper- ative paradoxical diplopia is to neutralize the angle of deviation with a prism. If the patient has diplopia with prism neutraliza- tion of the deviation, then the patient has ARC and the patient should be informed that postoperative diplopia will occur after the eyes are straightened. Fortunately, paradoxical diplopia is usually not so bothersome as true diplopia associated with normal retinal correspondence and, in most cases, paradoxical diplopia will vanish within a few weeks after surgery. Only in rare circumstances is postoperative paradoxical diplopia so bothersome that it interferes with everyday activities. Even so, in rare instances, persistent postoperative paradoxical diplopia has required a reoperation to recreate the initial strabismus to eliminate paradoxical diplopia. In cases where preoperative prism neutralization creates paradoxical diplopia that bothers the patient, one can prescribe press-on prisms (prism adaptation) to see if the diplopia will subside over several weeks. Bagolini striated lenses on a patient with a 20 PD esotropia and ARC are depicted in Figure 6-7A. The patient perceives a cross (normal response) even though there is an esotropia, because the line in the deviated eye passes through the pseudo- fovea. If a strabismic patient reports seeing a complete cross to Bagolini striated lenses, then they have ARC (Fig. 6-7B). This cortical reorganization of ARC is only present during binocular viewing and, when the dominant eye is covered, the patient reorients to the true anatomic fovea (Fig. 6-7C). ARC should not be confused with eccentric fixation. Remember, ARC is only chapter 6: sensory aspects of strabismus 185

A

B

C FIGURE 6-7A–C. Anomalous retinal correspondence (ARC) as tested with Bagolini lenses. (A) Bagolini lenses stimulate the right fovea (F) and left pseudo-fovea (PF). Note that the pseudo-fovea (PF) is nasal to the true fovea (F). (B) Retinal location of the Bagolini striation when the fovea (F) of the right eye is being stimulated and the pseudo-fovea (PF) of the left eye is being stimulated. Patient’s perception is a cross, as the pseudo-fovea (PF) corresponds to the true fovea (F). (C) When the right eye is occluded, the patient now fixates with the true fovea (F) of the left eye. Note that the pseudo-fovea has disappeared. Patient perceives a single line, which stimulates the visual center. 186 handbook of pediatric strabismus and amblyopia present during binocular viewing, whereas eccentric fixation represents a monocular loss of vision (amblyopia) and is present during both monocular and binocular viewing. ARC provides crude binocular vision with superimposition of retinal images; however, there is not true fusion. Patients with ARC do not have fusional vergence amplitudes, and they do not have stereoacuity. ARC can occur in association with intermittent strabismus. Some patients with intermittent exo- tropia, for example, have binocular vision with stereopsis when they are aligned but switch to ARC when they are tropic. In general, ARC is associated with good vision or only mild amblyopia. Harmonious ARC is the term used for the situation as described previously where the position of the pseudo-fovea completely compensates for the angle of strabismus (see Fig. 6- 6). Described another way, the strabismic deviation equals the pseudo-foveal offset from the true fovea. The amount of pseudo- foveal offset is termed the angle of anomaly, which is equal to the strabismic deviation (objective angle). Clinically, however, there are many cases in which the angle of strabismus does not exactly match the location of the pseudo-fovea so that the target image does not fall on the pseudo-fovea. This condition is called unharmonious ARC. In Figure 6-8A, the angle of the strabismus measures 20 PD (objective angle), but the pseudo-fovea is only 15 PD from the true fovea (angle of anomaly 15 PD). Thus, the image is falling 5 PD nasal to the pseudo-fovea. A 5 PD base-out prism over the right eye places the image on the pseudo-fovea and eliminates the diplopia. The discrepancy between the location of the pseudo-fovea and the location of the target image is called the subjective angle; in Figure 6-8B, the subjective angle is 5 PD. Note that neutralizing the subjective angle eliminates diplopia associated with unharmonious ARC, but neutralizing more than the subjective angle results in paradoxical diplopia (Fig. 6-8C). In these cases of unharmonious ARC, it is likely that the angle of strabismus has changed (usually increased) after the development of the pseudo-fovea. Most patients with unharmo- nious ARC suppress the target image so as not to experience diplopia. Others, perhaps those who had a change in the devia- tion off the pseudo-fovea in late childhood or adulthood, do expe- rience diplopia. Further discussion of unharmonious ARC and angle of anomaly is located under Amblyoscope, later in this chapter. chapter 6: sensory aspects of strabismus 187

A

B

C FIGURE 6-8A–C. Unharmonious ARC in a patient with esotropia. The pseudo-fovea (PF) is not in alignment with the retinal image in the devi- ated eye. (A) Patient perceives uncrossed diplopia or suppresses the image in the deviated eye. (B) A base-out prism is used to place the image on the pseudo-fovea (PF). Patient perceives a superimposed single image. A red filter in front of the right eye causes the image to appear pink, a com- bination of the clear image (left eye) and the red image (right eye). (C) A 20 PD prism is placed base-out in front of the deviated eye to place the image on the true fovea (F). Patient now has paradoxical diplopia and sees the red image on the contralateral side, causing crossed diplopia.

Practically speaking, the differentiation between harmo- nious versus unharmonious ARC is not of great clinical impor- tance; however, paradoxical diplopia after is of clinical concern. Adult patients with long-standing strabis- 188 handbook of pediatric strabismus and amblyopia mus should be examined for ARC by neutralizing the deviation with a prism.

Large Regional Suppression Children who have large-angle strabismus or severe unilateral retinal image blur develop a large suppression scotoma to elim- inate the image disparity (Fig. 6-9). Patients with large-angle constant strabismus (e.g., congenital esotropia), will have essen- tially no binocularity, not even peripheral fusion or ARC. Large regional suppression, however, is not always constant and can be intermittent. Patients with large-angle strabismus and large fusional vergence amplitudes (e.g., intermittent exotropia) have intermittent strabismus and intermittent regional suppression. These patients switch from a state of binocular fusion to monoc- ular vision and suppression. Another example of intermittent large regional suppression is seen in patients with congenital incomitant strabismus, where the eyes are straight in one field of gaze (Duane’s syndrome, or congenital superior oblique palsy). These patients have binocular fusion when their eyes are aligned with a compensatory face turn, but they suppress when they look into the field of gaze where they have strabismus. Patients with intermittent exotropia and Duane’s syndrome that have developed suppression do not have diplopia when they are tropic.

Horror Fusionis Normal sensory and motor fusion, once established, is usually permanent. Binocular fusion, however, can be lost if severe and sustained abnormal visual stimulation is acquired. Long-term occlusion of one eye, especially if it is the dominant eye, can result in a loss of binocular fusion in some patients. If this loss of binocular fusion occurs late in visual development or adult- hood, the patient will be too old to suppress. The inability to either fuse or suppress images results in intractable diplopia and is termed horror fusionis, or acquired disruption of cen- tral fusion. Causes of this rare syndrome include a unilateral acquired cataract occurring in older children and adults.2,4,6 In these cases, prolonged occlusion caused by a cataract appears to eliminate binocular fusion and, if the child is too old to sup- press, diplopia results. An acquired cataract in the dominant eye of an adult with previous strabismus or amblyopia can also cause chapter 6: sensory aspects of strabismus 189

FIGURE 6-9. Worth 4-dot in a patient with large regional suppression of the right eye. The two dots fall within the suppression scotoma, so the patient perceives three dots from the left eye.

horror fusionis. In these cases, prolonged occlusion of the dom- inant eye results in loss of preexisting suppression, leaving the patient with diplopia. In addition, horror fusionis can be caused by antisuppression therapy, such as forcing fixation with the nondominant eye in patients with strabismus. Antisuppression consists of training the strabismic patient to recognize the diplopia, which can be done by using dense red filters over the dominant eye to force fixation to the nondominant eye. Anti- 190 handbook of pediatric strabismus and amblyopia suppression is especially dangerous in patients with strabismus and poor fusion potential.

Prolonged Visual Plasticity The dogma regarding the relatively short span of visual central nervous system plasticity has come into question. Veteran stra- bismologists know that some adult patients with acquired stra- bismus can eventually learn to ignore or suppress their double vision. Do these patients actually develop suppression or do they consciously ignore their diplopia? In a study of acquired stra- bismus in adults, this author used the pattern visual evoked potential (VEP) to document suppression of visual cortical activity in adult patients with acquired strabismus.10 Another example of prolonged plasticity is seen in adults with ambly- opia, who can show significant improvement after losing vision in their good eye.1,7

Sensory Tests

DIPLOPIA TESTS Diplopia tests use one fixation target seen by both eyes. The target images fall on both foveas and corresponding retinal points if the eyes are aligned (Fig. 6-10). If strabismus is present, the target image falls on the fovea of the fixing eye and an extrafoveal point in the nonfixing eye (Fig. 6-11). A color filter is placed over one eye (usually red) or both eyes (usually red for right eye, green for left eye) to tint the image of each eye. By dis- tinctly tinting the retinal images of each eye, the examiner can tell which image corresponds to which eye. Lenses that place a streak of light on the retina (Maddox rod and Bagolini lens) are also used to stimulate the retina. Many diplopia tests disrupt fusion by obscuring, or even eliminating, peripheral fusion clues. Tests that disrupt fusion are referred to as dissociating tests. Table 6-1 lists different diplopia tests, with the most dissociating test listed first and the least dissociating test last. Note that under scotopic conditions tests that use filters, such as the Worth 4-dot test and red filter test, become extremely dissociating, because the only images seen by the patient are the test lights and peripheral fusion clues are lost. chapter 6: sensory aspects of strabismus 191

Red Filter Test Othotropia NRC

Penlight

LE RE

F F

L Center R

Binocular Perception

One Pink Light FIGURE 6-10. Red filter test in a normal patient with straight eye and normal retinal correspondence. Note that the image from the penlight falls on both foveas and the patient perceives a single binocular image. 192 handbook of pediatric strabismus and amblyopia

Red Filter Test R-Esotropia ARC

Penlight

LE RE

F FP

L Center R

Binocular Perception

One Pink Light FIGURE 6-11. Red filter test in a patient with a right esotropia and ARC. Red filter is placed in front of the right eye (RE) and the image falls on the pseudo-fovea (P) and fovea, representing corresponding retinal points in a patient with ARC. The patient has a single binocular perception and sees one pink light. LE, left eye. chapter 6: sensory aspects of strabismus 193

TABLE 6-1. Types of Diplopia Tests. Most dissociating Maddox rod Dark red filter Worth 4-dot with room lights out Worth 4-dot with room lights on Least dissociating Bagolini striated lenses

SPECIFIC DIPLOPIA TESTS

RED FILTER TEST One of the simplest diplopia tests is the red filter test. Place a red glass over one eye and direct the patient to fixate on a single light source, or an accommodative fixation target. Patients with straight eyes and normal retinal correspondence will see one pinkish-red light (see Fig. 6-10). If a phoria is present, the red filter may dissociate the eyes and then the patient will man- ifest their deviation and see double. The denser the red color, the more dissociating the test. Another way to make the stan- dard red filter test more dissociating is to turn down the room lights. In dim illumination, the eye behind the red filter will only see the light source, not background objects in the room, which will eliminate peripheral fusion clues. The red filter test is useful for identifying NRC, ARC, and suppression. Esotropia with NRC causes uncrossed diplopia, with the red light seen on the same side as the red filter (see Fig. 6-1). Alternately, exotropia with NRC is associated with crossed diplopia as the red light is opposite to the red filter (see Fig. 6-2). When the deviation is neutralized with a prism, the diplopia disappears and the images will be superimposed. Patients with ARC will generally see one light, even though they have strabismus, because they use a pseudo-fovea. In Figure 6-11, the red light falls on the pseudo-fovea of the right eye. This image is cortically superimposed with the foveal image of the left eye to produce the perception of one pink light. If partial or full prism neutralization of the deviation results in diplopia, then the patient has ARC. Strabismus associated with suppression results in the per- ception of a single light, either a red or a white light, depending on which eye is fixing. In Figure 6-12, the left eye is fixing, so the patient sees one white light and suppresses the red light falling on the right retina. If a dark red filter is placed over the 194 handbook of pediatric strabismus and amblyopia

Red Filter Test (Esotropia and Suppression RE) NRC

Penlight

Red Filter

LE RE

F F Suppression Scotoma L Center R

Binocular Perception LE

One White Light FIGURE 6-12. Red filter test in a patient with childhood esotropia who developed suppression and a fixation preference for the left eye. Patient fixes left eye with a suppression scotoma of the right eye. Note that the retinal image of the penlight falls within the suppression scotoma, so the patient only perceives one white light from the left eye. chapter 6: sensory aspects of strabismus 195

fixing left eye, then fixation switches to the right eye, and the left eye is suppressed (Fig. 6-13). Patients who alternate fixation may report seeing two lights: a red light alternating with a white light. When a child with a manifest strabismus claims to see two

Red filter over LE

Penlight

Dark red filter

LE RE

F F

Suppression Scotoma L Center R

Binocular Perception RE

One White Light FIGURE 6-13. A dark red filter is placed over the left eye to shift fixa- tion to the right eye. With the right eye fixing, patient suppresses the image in the left eye and perceives one white light from the right eye. 196 handbook of pediatric strabismus and amblyopia lights, be sure to distinguish between diplopia, where the red and white lights are seen simultaneously, and alternating sup- pression, where one light is seen at a time. Partial or full prism neutralization of the strabismus will not result in diplopia. The patient with suppression will continue to see just one light.

VERTICAL PRISM RED FILTER TEST/SUPPRESSION VERSUS ARC Another way ARC can be distinguished from NRC in patients with suppression is by placing a red vertical prism (usually 15 PD base-down) over the deviated eye. A vertical prism causes patients with ARC to see two vertically displaced images, with the red light directly over the white light (Fig. 6-14). The lights are vertically aligned because the light in the deviated eye is over the pseudo-fovea that corresponds to the true fovea of the fixing eye. When a vertical prism is introduced to the deviated eye of a patient with central suppression and NRC, the patient reports seeing two lights that are horizontally and vertically displaced because there is no pseudo-fovea and the center of reference is the true fovea of each eye (Fig. 6-15).

WORTH 4-DOT The Worth 4-dot test consists of two green lights, one red light, and one white light (Fig. 6-16). The patient wears red/green glasses, usually with the red lens over the right eye, and views a Worth 4-dot flashlight at one-third of a meter, or a Worth 4- dot light box at 6 m (20 ft). The near Worth 4-dots are separated by 6° at near (flashlight at 1/3 m) and by 1.25° for the distance (light box at 6 m). When the test is performed with the room lights out, the white dot is the only binocular fusion target, as it is the only light seen by both eyes. Green lights are seen through the eye behind the green filter, and the red light is seen with the eye with the red filter. If the room lights are turned on, however, the patient can see the room environment with both eyes, including the Worth flashlight and examiner, thus provid- ing strong fusion clues; this is why Worth 4-dot testing in the dark is much more dissociating than testing with the room lights on. The normal fusion response is seeing four lights, two red and two green. Another normal response is one red light, two green lights and one light that flickers between red and green. The light that flickers is the white light that is seen by both chapter 6: sensory aspects of strabismus 197

Esotropia ARC

Penlight

L-ET RE

F P F

F

Red prism base down

L Center R

Binocular Perception

Vertical Diplopia with two lights in horizontal alignment FIGURE 6-14. Patient with esotropia and ARC is presented with a base- down vertical prism and a red filter over the left eye. The prism deflects the retinal image below the pseudo-fovea (P) and the patient perceives two images: vertically, one on top of the other. Remember, the pseudo- fovea (P) is the center of vision during binocular viewing. 198 handbook of pediatric strabismus and amblyopia

Esotropia NRC Suppression

Penlight

L-ET RE

ET

F F

F

Red prism base down

L Center R

Binocular Perception

Vertical and Uncrossed Diplopia FIGURE 6-15. Patient with esotropia and suppression of left eye. A base- down prism is placed in front of the left eye, which displaces the retinal image inferiorly and out of the central scotoma. The patient perceives two images: vertically and horizontally displaced. Note that there is no pseudo-fovea (F) and the true foveas are at the center of vision. chapter 6: sensory aspects of strabismus 199

FIGURE 6-16. Worth 4-dot test in a normal patient with straight eyes. Three lights are projected to the left eye and two lights to the right eye. Patient fuses the two images and perceives four lights. eyes, the flicker being color rivalry. Patients with acquired stra- bismus and diplopia will see five lights: three green and two red. Patients with cortical suppression report seeing either three green lights or two red lights, depending on which eye is fixing. In Figure 6-9, the left eye is fixing and the right eye is suppressed so the patient sees three green lights. If the right eye was the preferred eye and the left eye was suppressed, then the patient would see two red lights. Patients who alternate fixation usually describe seeing two red lights, alternating with three green 200 handbook of pediatric strabismus and amblyopia lights. A few patients, however, will report the sum total of the alternating lights, that is, five lights. Thus, alternating suppres- sion can be confused with diplopia, because patients with diplopia also report seeing five lights. Patients with large sco- tomas ( greater than 6°) will suppress both the distance (central field) and near (peripheral field) Worth 4-dot. Patients with the monofixation syndrome have a small central suppression scotoma (5°) and peripheral fusion. They fuse, or see, four lights for the near Worth 4-dot (which subtends 6°) because the dots fall outside the scotoma (Fig. 6-17), but sup-

FIGURE 6-17. Near Worth 4-dot test in a patient with monofixation syndrome and 8 PD (4°) esotropia. The near Worth 4-dot subtends 6° and the dots fall outside the scotoma. Patient perceives four dots. chapter 6: sensory aspects of strabismus 201

FIGURE 6-18. Distance Worth 4-dot test in a patient with monofixation syndrome and esotropia of 8 prism diopters. The distance Worth 4-dot subtends 1.25° and two dots fall within the central suppression scotoma. Therefore, patient perceives three dots from the left eye and no dots from the right eye. press the distance Worth 4-dot (which subtends only 1.25°) as the dots fall within the scotoma (Fig. 6-18). One of the best uses of the Worth 4-dot test is to identify the monofixation syndrome (i.e., central suppression and peripheral fusion) in a patient with a small-angle strabismus. The results of this test will tell the examiner if there is peripheral fusion that can be present even if there is no discernible stereoscopic vision. Remember, it is important to leave the room lights on when performing the Worth 4-dot test if the goal is to promote fusion. 202 handbook of pediatric strabismus and amblyopia

With the room lights on, the patient can see background objects in the room with both eyes, providing binocular peripheral fusion clues. If the lights are dimmed or turned off, however, only the Worth lights can be seen and the only target seen by both eyes is the single white dot. Because of the lack of periph- eral fusion clues, the Worth 4-dot test becomes extremely dis- sociating in the dark. Once one realizes the dissociating power of the dark, one can use this phenomenon to estimate how well a patient fuses. If a patient can maintain fusion of the Worth 4- dot test with lights out, then this indicates strong motor fusion. On the other hand, if dimming the lights changes the response from fusion to suppression or diplopia, this reveals relatively weak motor fusion. Patients with intermittent exotropia who have weak motor fusion manifest their deviation when the lights are dimmed. The Worth 4-dot flashlight can be used to plot the size of suppression scotomas. By moving the flashlight closer to the patient, the lights subtend a larger angle (i.e., stimulate more peripheral retina) and by moving the flashlight farther away, the lights subtend a smaller angle (i.e., stimulate more central retina). Table 6-2 describes the stimulus angle for the Worth 4- dot flashlight at various distances from the patient.

BAGOLINI LENSES Bagolini striated lenses are clear with a linear scratch through the center of each lens that provides a streak of light on the retina when viewing a bright light (see Fig. 6-5). One lens is placed over each eye, and the lenses are oriented obliquely at 45° and 135°. Because the lenses are otherwise clear, they are not dissociating. Bagolini lenses, therefore, have the advantage of providing a free binocular view without dissociation. Patients with straight eyes and NRC, and those with harmonious ARC, will report seeing a cross (Fig. 6-19A). Remember, with ARC, one line is on the true fovea and the other line falls on the

TABLE 6-2. Stimulus Angle for Worth 4-Dot Flashlight. Flashlight distance from patient Worth 4-dot angle 1/6 m 12° 1/3 m (14 in.) 6°a 1/2 m 4° 1 m 2° aStandard near Worth 4-dot. chapter 6: sensory aspects of strabismus 203

FIGURE 6-19A–E. Patient perception of Bagolini testing. (A) A cross is perceived in orthotropia with normal retinal correspondence or strabis- mus with ARC. (B) Patient with strabismus and large suppression scotoma sees one line. (C) Patient with monofixation syndrome and small central scotoma will see one continuous line and one line broken in the center that corresponds to the eye with the suppression scotoma. (D) Patient with esotropia and uncrossed diplopia reports a “V” configura- tion. (E) Patient with exotropia and crossed diplopia reports an “A” configuration.

pseudo-fovea (see Fig. 6-7). Patients who have large regional suppression will report seeing only one line (Fig. 6-19B). The monofixation syndrome, on the other hand, is associated with a cross, but one line will have a central gap (Figs. 6-19C, 6-5). Patients with NRC, , and diplopia will show the response of either an “A” or a “V.” Because esotropia is associ- ated with uncrossed diplopia, esotropia will cause the right line to move to the right and the left line to move to the left, creating a “V” (Fig. 6-19D). Exotropia produces an “A” because exotropia is associated with crossed diplopia, with the right line moving to the left and the left line moving to the right (Fig. 6-19E). 204 handbook of pediatric strabismus and amblyopia

MADDOX ROD TEST The Maddox rod can be used for identifying horizontal, vertical, and, especially, torsional deviations. The Maddox rod has a washboard appearance as it is made up of multiple cylindrical high plus lenses stacked on top of each other. When the patient views a light through the Maddox rod, a linear streak of light oriented 90° to the cylindrical ribs of the Maddox rod is seen. The single Maddox rod test is performed by placing the Maddox rod over one eye and having the patient view a penlight. The Maddox rod is aligned so the streak is vertical to detect hori- zontal deviations and then horizontal for vertical deviations. If the streak of light passes through the penlight, the patient is orthophoric, or has harmonious ARC. This is one of the most dissociating tests, because the images to each eye are totally dif- ferent and there are essentially no binocular fusion clues. The Maddox rod test is so dissociating that it will cause patients with normal bifoveal fusion to manifest their phoria. Because of this, the Maddox rod test, and dissociating tests in general, do not distinguish between phorias and tropias. To make the diagnosis of phoria versus tropia, one must assess the eye alignment objectively before administering the dissociating diplopia test. The Maddox rod test can also be used to measure torsion (as described in Chapter 5).

Haploscopic Tests In contrast to diplopia tests where there is one stationary fixa- tion target that is viewed by both eyes, haploscopic tests have two fixation targets, one for each eye, and the targets can be moved separately to align with each fovea. A haploscopic pres- entation means each eye receives its own visual stimulus. There are various ways to separately stimulate each eye. One way to create haploscopic vision is to place a mirror in front of each eye, with the mirrors angled so the right eye sees the right tem- poral side and the left eye sees the left temporal side. Mirror sep- aration of vision is the principle of the amblyoscope. Another commonly used method is to give the patient color-tinted glasses with one eye receiving a red filter and the fellow eye a green filter. Two movable targets are presented on a white screen: one red and one green. The eye with the red filter sees only the red target and the eye with the green filter sees only the green target; thus, separate visual stimuli are presented to each eye; this is the principle of the Lancaster red/green test. If chapter 6: sensory aspects of strabismus 205 strabismus is present, either the mirrors can be angled or the red/green targets moved so the fixation target is aligned with each fovea. Haploscopic tests include the Lancaster Red/Green Test and the amblyoscope. The Lancaster Red/Green test is used to measure the angle of strabismus (see Chapter 5; Fig. 5-14). Note that the Worth 4-dot test is partially haploscopic because some of the objects in the visual field are seen by both eyes. The Worth 4-dot test is not a true haploscopic test, as targets are not independently movable to each eye and cannot be aligned with each fovea.

AMBLYOSCOPE The amblyoscope provides a haploscopic view, allowing presen- tation of images to each eye independently. Two mirrors at the elbow of the amblyoscope arms reflect images from transparent picture slides into each eye (Fig. 6-20). The arms can be moved to measure either subjective or objective angle. The subjective angle is the amount in degrees the examiner must move the amblyoscope arms to allow the patient to see the two pictures

FIGURE 6-20. Amblyoscope testing a patient with normal retinal corre- spondence (NRC) and orthotropia. A dot is a target for the left eye and a ring is the target for the right eye. Patient sees the dot inside the ring without moving the arms of the amblyoscope. 206 handbook of pediatric strabismus and amblyopia as being superimposed. The objective angle is measured by alter- nating the target presentation from right eye to left eye, moving the arms of the amblyoscope until there is no refixation eye movement. The objective angle equals the deviation as meas- ured by the alternate prism . The subjective angle is determined under binocular viewing conditions whereas the objective angle is measured during monocular viewing.

NORMAL RETINAL CORRESPONDENCE In a strabismic patient with NRC and diplopia, the subjective and objective angles are the same (Fig. 6-21) because patients with NRC always use the fovea as the center of reference. Patients with NRC and dense large regional suppression will not have a measurable subjective angle because they suppress one eye, making subjective superimposition of the images impos- sible. The subjective angle can be measured in patients with the monofixation syndrome and a small central suppression scotoma by using targets that stimulate the peripheral retina.

FIGURE 6-21. Patient with NRC and esotropia. The arms of the amblyoscope are angled so the image falls on each fovea and the patient perceives the dot inside the circle. Each arm is moved 20 (10°) for a total of 40 . chapter 6: sensory aspects of strabismus 207

FIGURE 6-22. Patient with harmonious ARC and right esotropia. The arms of the amblyoscope do not have to be angled for the patient to see the dot inside the ring, as the pseudo-fovea (P) is directly aligned with the ring target. The patient perceives the dot in the center of the circle with the arms of the amblyoscope parallel aligned to zero.

ANOMALOUS RETINAL CORRESPONDENCE (HARMONIOUS) Patients with strabismus and harmonious ARC have a signifi- cant objective angle, but the subjective angle is zero. The sub- jective angle is zero (or close to zero) because the subjective angle is measured under binocular conditions and reflects the alignment based on the relationship between the true fovea of the fixing eye and the pseudo-fovea of the deviated eye. Because patients with harmonious ARC have the pseudo-fovea posi- tioned to compensate for the angle of deviation, there is no sub- jective misalignment. Patients with harmonious ARC will see the targets from each eye as superimposed with the amblyoscope arms set to zero (parallel) even though there is a large objective angle (Fig. 6-22). The objective angle is measured by alternate cover testing, blocking the vision of each eye (monocular viewing) so the objective angle reflects the misalignment based on the true fovea. The displacement of the pseudo-fovea off the true fovea is called the angle of anomaly. Because the location 208 handbook of pediatric strabismus and amblyopia of the pseudo-fovea completely compensates for the objective deviation in harmonious ARC, the subjective angle is zero, and the objective angle equals the angle of anomaly. For example, in Figure 6-22, the objective angle is ET 20 PD and the subjective angle is zero. The angle of anomaly (i.e., distance of the pseudo- fovea from the true fovea) is 20 PD (200). In patients with unharmonious ARC, the pseudo-fovea is located in a position that does not fully compensate for the objective deviation. These patients will see double or will sup- press the image that does not fall on the pseudo-fovea (Fig. 6-23: “I” image in right eye). The subjective angle is measured by moving the arms of the amblyoscope until the two images are superimposed. When the images are superimposed, the image of

FIGURE 6-23. Patient with unharmonious ARC and 30 PD of esotropia. The arms of the amblyoscope are set at zero and are not angled. As the image (I) is falling nasal to the pseudo-fovea (P), the patient perceives uncrossed diplopia (as diagrammed in the rectangle at the bottom of the figure). If the arm of the amblyoscope in front of the right eye was moved 10° in to place the image on the pseudo-fovea (P), the patient would per- ceive the ring around the dot. chapter 6: sensory aspects of strabismus 209 the fixing eye is on the true fovea, and the image in the nonfix- ing eye is on the pseudo-fovea. The subjective angle is the number of degrees from the zero position the amblyoscope arm needs to move to place the image on the pseudo-fovea. For example, in Figure 6-23, the subjective angle (I-P, right eye) is 10 PD, and the objective angle (I-F, right eye) is 30 PD. Because the angle of anomaly (P-F) is equal to the objective angle minus the subjective angle, the angle of anomaly is 20 PD (3010). The amblyoscope is a useful tool as it can measure fusional vergence amplitudes, angle of deviation, area of suppression, retinal correspondence, and even torsion. Some degree of instru- ment convergence, however, is usually present when using the amblyoscope.

AFTERIMAGE TEST The afterimage test is a fovea-to-fovea sensory test that does not use a haploscopic apparatus, but each eye is stimulated sepa- rately. Each fovea is marked individually during monocular viewing with a linear strobe light that bleaches the retina; this causes a linear afterimage shadow through the true fovea that lasts approximately 10 s. The center of the linear strobe light is masked to spare the fovea; thus, the afterimage line has a break in the middle. Testing is performed by having the patient occlude one eye while the other eye fixates on the central masked part of the strobe light held vertically in front of the patient (Fig. 6-24). The fixing eye is stimulated to produce a ver- tical afterimage. Next, the fellow eye is stimulated with a hor- izontally oriented strobe light while the first eye is covered (Fig. 6-24B). The occluder is quickly removed, and the patient is asked where they see the afterimage lines while they are binocularly viewing (Fig. 6-24C). Because the stimulus is presented under monocular conditions, the stimulus always marks the true fovea of each eye unless there is eccentric fixation from dense ambly- opia. Patients with NRC will, therefore, always see a cross whether they are orthophoric, esotropic, exotropic, or hyper- tropic because their center of reference is the fovea under monocular or binocular conditions (Fig. 6-25A,B). Patients with ARC however, use their true fovea during monocular viewing but, during binocular viewing, the deviated eye switches to the pseudo-fovea. Consequently, patients with ARC have each fovea marked by the monocular afterimage, but when binocular vision is reestablished, the pseudo-fovea takes over as the center of A

B

C AB

CD FIGURE 6-25A–D. Perception of afterimage test in patients with (A) NRC orthotropia, (B) NRC and strabismus, (C) ARC esotropia, and (D) ARC exotropia. Note that the stimulation for the afterimage test occurs under monocular conditions and that the light always tags the fovea, even in patients with ARC. After the stimulation, the patient is again given binocular vision, so the patient switches back to the pseudo-fovea and the image tagged on the fovea appears to be in an eccentric location (C and D).

FIGURE 6-24A–C. Afterimage test of a patient with NRC. If the patient has NRC, the results of the afterimage test are the same whether the patient has straight eyes, esotropia (ET), exotropia (XT), or a hyperdevia- tion. (A) Right eye is stimulated with a vertical strobe while the left eye is covered. (B) Left eye is stimulated with a horizontal strobe light while the right eye is covered. (C) The cover is removed and the patient reports seeing a cross.

211 212 handbook of pediatric strabismus and amblyopia reference for the deviated eye. As the pseudo-fovea is the center of reference, the afterimage marked on the true fovea is perceived as coming from the peripheral visual field. With esotropia, the fovea is temporal to the pseudo-fovea and tem- poral retina projects to the opposite hemifield, so the right afterimage is seen on the left (Fig. 6-25C). Exotropia is just the opposite, with the fovea nasal to the pseudo-fovea and nasal retina projecting to the ipsilateral hemifield, so the right afterimage is seen on the right (Fig. 6-25D).

Other Tests for Suppression and Fusion

VECTOGRAPHIC TEST The vectographic test is an excellent test for suppression. The test consists of two superimposed polarized slides of letters that are projected onto an aluminized screen which reflects the images while preserving polarization. The patient is asked to read the letters on the screen while wearing polarized glasses. The polarization of the glasses and the projected slides are ori- ented so some of the letters are only seen by the right eye, some are only seen by the left eye, and some are seen by both eyes (Fig. 6-26). Patients with normal bifoveal fusion will see all the letters. If suppression is present, the letters projected only to the suppressed eye will not be seen (Fig. 6-27). Some patients with suppression will alternate fixation and will see all the letters, although viewing them separately.

FOUR BASE-OUT TEST This test is performed by first placing a 4 PD base-out prism over one eye. In normal subjects, the 4 base-out test induces fusional convergence. Remember, there are two movements to prism convergence: first, a version movement of both eyes in the direc- tion of the apex of the prism, and second, a fusional vergence movement of the eye without the prism in toward the nose. With the 4 base-out test, the examiner must look carefully for the second convergence movement, as it is the sign of fusion. Patients without motor fusion and large regional suppression show no movement of either eye when the prism is placed over the nondominant eye (Fig. 6-28A) and a version (not vergence) movement of both eyes in the direction of the apex of the prism when the prism is placed over the fixing eye (Fig. 6-28B). chapter 6: sensory aspects of strabismus 213

FIGURE 6-26. Diagrammatic representation of vectograph with polarized glasses in place and lenses oriented 90° to each other. Letters are projected to a screen through two polarized lenses, which are also oriented 90° to each other and match the orientation of the glasses. In this patient with normal binocular vision, the left eye sees AC, right eye sees AB, and the perception is ABC, which is noted in the rectangle at the bottom of the figure. 214 handbook of pediatric strabismus and amblyopia

FIGURE 6-27. Diagram of vectograph examination of a patient with a suppression scotoma, left eye. In this case, the patient only sees images from the right eye and reports seeing an AB.

Patients with the monofixation syndrome and a small central scotoma usually show no movement when the 4 PD prism is placed over the nondominant eye. Because these patients have peripheral fusion, monofixators occasionally show a normal fusional convergence movement. A prism over the fixing eye always results in a version movement in monofixa- chapter 6: sensory aspects of strabismus 215 tors, and some will show fusional convergence movement as well. Normal patients with bifoveal fusion often show atypical responses to the 4 base-out test.5 Some normals fail to fuse the 4 PD base-out prism, showing an initial version movement but no secondary fusional convergence movement. These patients often alternate fixation and report alternating diplopia. Other normals seem to ignore the induced phoria and show no move-

A

B FIGURE 6-28A,B. (A) Esotropia, left eye fixing, right eye deviated with large suppression scotoma. Placing the 4 base-out prism in front of the deviated right eye produces no movement of either eye, because the image falls within the suppression scotoma. (B) Placing the 4 base-out prism in front of the fixing eye results in a version movement, with both eyes moving in the direction of the apex of the prism, because there is no sup- pression scotoma and the movement of the image is perceived. 216 handbook of pediatric strabismus and amblyopia ment when the 4 base-out prism is placed over one eye. Thus, a secondary fusional convergence movement on 4 base-out prism testing indicates fusion (central fusion or even peripheral fusion), but because of frequent atypical responses in normals, absence of a convergence movement does not necessarily mean an absence of fusion.

References

1. Ellis FD, Schlaegel TF. Unexpected visual recovery: organic ambly- opia? Am Orthopt J 1991;31:7. 2. Kushner BJ. Abnormal sensory findings secondary to monocular in children and strabismic adults. Am J Ophthalmol 1986; 102(3):349–352. 3. Parks MM. The monofixation syndrome. Trans Am Ophthalmol Soc 1969;1242–1246. 4. Pratt-Johnson JA, Tillson G. Intractable diplopia after vision restora- tion in unilateral cataract. Am J Ophthalmol 1989;107:23. 5. Romano PE, von Noorden GK. Atypical responses to the four-diopter prism test. Am J Ophthalmol 1969;67:935. 6. Sharkey JA, Sellar PW. Horror fusionis: a report of five patients. J Am Optom Assoc 1999;667(12):733–739. 7. Vereecken EP, Brabant P. Prognosis for vision in amblyopia after the loss of the good eye. Arch Ophthalmol 1984;102:220. 8. Wong AMF, Lueder GT, Burkhalter A, Tychsen L. Anomalous retinal correspondence: neuroanatomic mechanism in strabismic monkeys and clinical findings in strabismic children. JAAPOS 2000:168–174. 9. Wright KW, Fox BES, Erikson KJ. P-VEP evidence of true suppression in adult onset strabismus. J Pediatr Ophthalmol Strabismus 1990;27: 196–201. 10. Wright KW, Hwang JM. Diplopia and strabismus after retinal and glaucoma surgery. Am Orthopt J 1994;44:26–30.