Fellow Eye Deficits in Amblyopia

1Crystal Charity Ball Pediatric Vision Laboratory, Retina Foundation of the Southwest, Dallas, TX, USA

2Department of Ophthalmology, UT Southwestern Medical Center, Dallas, TX, 11 USA

1Crystal Charity Ball Pediatric Vision Laboratory, Retina Foundation of the Southwest, Dallas, TX, USA

3Department of Ophthalmology and Visual Sciences, University of British Columbia, Vancouver, British Columbia, Canada

Amblyopia is a neurodevelopmental disorder of the visual system, as a result of discordant visual experience during infancy or early childhood. Because amblyopia is typically defined as monocularly reduced visual acuity accompanied by one or more known amblyogenic factors, it is often assumed that the fellow eye is normal and sufficient for tasks like reading and eye-hand coordination. Recent scientific evidence of ocular motor, visual, and visuomotor deficits that are present with fellow eye monocular viewing and with binocular viewing calls this assumption into question. This clinical update reviews the research that has revealed fellow ocular motor and visual deficits and the effect that these deficits have on an amblyopic child’s visuomotor and visuocognitive skills. We need to understand how to prevent and rehabilitate the effects of amblyopia not only on the nonpreferred eye but also on the fellow eye.

Amblyopia is a neurodevelopmental disorder of the visual system, as a result of discordant visual experience during infancy or early childhood. The most common causes of amblyopia are strabismus and anisometropia. It is widely appreciated that stereoacuity is disrupted in amblyopia and that interocular suppression plays a central role in causing amblyopia. Yet, because amblyopia is typically defined as monocularly reduced visual acuity accompanied by one or more known amblyogenic factors, it is often assumed that the fellow eye is normal and sufficient for tasks like reading and eye-hand coordination. Recent scientific evidence of ocular motor, visual, and visuomotor deficits that are present with fellow eye monocular viewing and with binocular viewing that calls this assumption into question are reviewed here.

Binocular vision relies on balanced visual input from the two eyes, as well as the ability of the eyes to make conjugate (saccades) and disconjugate (vergence) eye movements to fixate a target and maintain gaze. When binocular vision is disrupted early in life by strabismus, anisometropia, or amblyopia, a host of ocular motor deficits can occur, including fixation instability and abnormal saccades. In general, impaired ocular motor function is more pronounced when viewing with the non-preferred amblyopic eye, and when the visual acuity or stereoacuity deficit is severe.1–4 Yet, ocular motor deficits are also present when viewing with the fellow eye, even in nonamblyopic individuals with strabismus.5–7 Reduced visual acuity is present only in the amblyopic group, while both amblyopic and nonamblyopic individuals with strabismus or anisometropia have experienced binocularly discordant visual input during the critical period of visual maturation, suggesting that the fellow eye deficit is a consequence of discordant binocular experience, not the visual acuity deficit. Studies examining fellow eye deficits in amblyopic and nonamblyopic individuals with strabismus or anisometropia will be reviewed here.

During normal fixation, the eyes constantly make small, involuntary movements such as microsaccades, slow drifts, and tremors that aid in maintaining fixation and that prevent image fading.8–11 Remarkably, binocularity in the normal visual system is not affected by these eye movements. When these involuntary eye movements become excessive, instability occurs in the ability to maintain fixation and visual function is disrupted. Fixation instability is a common consequence of strabismus, anisometropia, and amblyopia. Instability associated with these pediatric eye conditions is typically composed of abnormal fixational saccades, ocular drift, and fusion maldevelopment nystagmus.1,4,8–10,16 Although amblyopia is associated with larger fixation instability, amblyopia is not a necessary condition for instability as it is also found in nonamblyopic strabismus.1–6,13,17

Research to date has typically focused on fixation instability under monocular viewing conditions with inconsistent results. Some studies have reported fellow eye stability with the amblyopic eye occluded.2,3,16,17 Other studies report increased fellow eye instability compared with controls.4,6,13,18,19 However, smaller angles of deviation and preserved binocular function may lessen instability.13 Unpublished monocular viewing data from the cohort described by Kelly et al20 also show amblyopic and nonamblyopic children with strabismus and/or anisometropia have larger fellow eye instability than controls (Figure 1).

Unpublished monocular viewing data from the cohort described in Kelly et al19 showing larger mean fellow eye instability for 85 amblyopic children (light gray bars) and 55 nonamblyopic children with strabismus or anisometropia (white bars), compared with 43 normal control children (dark grey bars). Error bars represent ±SE.

*significantly different than controls (pOpen in a separate windowFigure 2

Mean fellow eye instability and vergence instability during binocular viewing for 98 amblyopic children (light gray bars), 62 nonamblyopic children with strabismus or anisometropia (white bars), and 46 normal control children (dark grey bars). Amblyopic and nonamblyopic children exhibited larger fixation and vergence instability compared to controls. Error bars represent ± SE. *significantly different than controls (pOpen in a separate windowFigure 3

Left: global motion stimuli with 100% coherence (top) and 75% coherence (bottom). Right: motion-defined form stimuli with 100% coherence (top) and 75% coherence (bottom). Arrows were added to illustrate the direction of motion of each dot. The dotted-line boxes were added to illustrate the target shape. Neither the arrows nor the boxes were present in the actual stimulus displays.

Fellow eye global motion deficits have been reported in several studies of amblyopic children and adults,39–41 but there also are several studies that report few or no fellow eye deficits.42,43 (Figure 4) The discrepancies in results of various global motion studies appear to depend on the specific spatiotemporal parameters of the visual stimuli, requiring prior identification of the parameters that revealed an amblyopic eye deficit in order to observe the fellow eye deficit.41

% of children with amblyopia who had a deficit in perception of global motion direction (left) or motion-defined form orientation (right) when viewing with their fellow eye, compared with controls. Thresholds for both tasks were measured by the minimum percentage of coherently moving signal dots required for accurate discrimination.

Up to 40% of amblyopic children have been reported to have a fellow eye deficit in perceiving motion-defined form.43–45 Unlike global motion, fellow eye motion-defined form deficits are reported consistently across studies of amblyopic children and adults, despite some variations in visual stimuli. (Figure 4) Fellow eye motion-defined form deficits have been reported to be resistant to rehabilitation by patching,44 but were responsive to binocular amblyopia treatment. 46

Reading is a vision-reliant ability fundamental to academic achievement. Saccades during reading allow us to move forward and regress backward through text. Fixations, or pauses, occur during reading as decoding of phonemes occurs. Increased fixation duration or abnormal saccades could result in slower reading that, in turn, could be detrimental to academic performance and learning. Most studies of reading by amblyopic children have been conducted with monocular viewing, comparing amblyopic eye versus fellow eye reading performance to determine whether the treated amblyopic eye provides a useful “spare eye” in the event that the fellow eye can no longer be used for reading.47–49 More recently, monocular reading speed for the fellow eye has been studied; the fellow eye has decreased reading speed in strabismic and anisometropic amblyopia relative to monocular reading in visually normal children.48,50,51 Slower monocular reading with the fellow eye is associated with an abnormally increased number of saccades.51

With binocular viewing by amblyopic children and adults, there are several reports of slow reading of sentences and words, and slow reading of paragraphs of text projected on a distant screen.48–50 More recently, natural, binocular silent reading of age-appropriate print paragraphs at habitual reading distance has been assessed in amblyopic children.52,53Amblyopic children with strabismus or anisometropia read slowly compared with controls and nonamblyopic strabismic children.52,53 Unlike the earlier studies, this more recent work clearly identified that amblyopia alone was sufficient to cause slow reading; reading performance was not related to severity of amblyopia, nor to diagnosis (strabismic, anisometropic). Further, data from Kelly et al51 reported similar reading rate and number of forward saccades for binocular reading versus fellow eye reading in amblyopic children, suggesting that rather than binocular inhibition (i.e., amblyopic eye interference during binocular reading), slow reading is due to a fellow eye deficit even when reading with two eyes (Figure 5).

Mean reading rate (words per minute) and number of forward saccades (per 100 words) assessed with the Readalyzer ® during binocular viewing (grey bars) and fellow eye viewing (white bars) for 49 amblyopic children No differences were found (ps≥0.50). Error bars represent ± SE. The dashed line represents previously published control data for binocular reading.52

Importantly, reading comprehension did not differ significantly between amblyopic children and controls, nor did fixation duration or number of regressive eye movements.52–54 Taken together, these findings suggest that amblyopic children did not read slowly because they had dyslexia or a learning disability. In fact, amblyopic children show low (Open in a separate windowFigure 6

Mean standard scores for manual dexterity tasks completed during binocular viewing for 129 amblyopic children (light gray bars), 47 nonamblyopic children with strabismus (white bars), and 40 normal control children (dark grey bars). Amblyopic children had lower scores for all three tasks compared to controls. Nonamblyopic children with strabismus had lower scores on the bimanual and drawing trail tasks compared with controls. Error bars represent ± SE.

*significantly different than controls (pOpen in a separate windowFigure 7

% of amblyopic children who have a fellow eye deficit for motion-defined form perception in subgroups with randot stereoacuity of 1.6–2.9 log arcsecs (Yes) vs nil stereoacuity (No), with macular/foveal fusion by Worth 4-dot test (Yes) vs peripheral/no fusion, and with prior binocular amblyopia treatment (Yes) vs no prior binocular treatment (No).

Fellow eye deficits prompt us to reconsider whether amblyopia is adequately characterized as a monocular visual acuity deficit, and whether treatment by occlusion of the fellow eye, or occlusion coupled with monocular perceptual learning is optimal. Fellow eye motion-defined form perception deficits have been reported to be resistant to rehabilitation by patching44 but responsive to binocular amblyopia treatment.46 (Figure 7). More effective treatments for amblyopia may target suppression, by requiring integration of information between the two eyes to play dichoptic games or watch dichoptic videos. Like occlusion therapy, binocular treatment results reported to date are generally positive for young children 81–87 but less effective for older children due to poor compliance and/or intractable residual amblyopia.88–90

For many years, the fellow eye was considered to be normal and study after study assessed the child’s ability to see, read, or perform visuomotor tasks using the amblyopic eye to determine whether it was a useful spare eye. The overarching goal was to evaluate whether the monetary and personal cost of years of occlusion therapy were worth the benefit of a few lines gain in visual acuity. Now the paradigm has shifted; we have discovered that the fellow eye also has visual deficits and that these deficits affect an amblyopic child’s visuomotor and visuocognitive skills. We need to understand how to prevent and rehabilitate the effects of amblyopia not only on the nonpreferred eye but also on the fellow eye.

Supported in part by a grant from the National Eye Institute EY022313

None of the authors have a financial interest in the material included in this Clinical Update.