Vision with one eye: a review of visual function following unilateral enucleation

Spatial Vision, Vol. 21, No. 6, pp. 509–529 (2008)! Koninklijke Brill NV, Leiden, 2008.Also available online - www.brill.nl/sv

Vision with one eye: a review of visual function followingunilateral enucleation

JENNIFER K. E. STEEVES 1,2,3,4,!, ESTHER G. GONZÁLEZ 1,3,4,5

and MARTIN J. STEINBACH 1,2,3,4,5

1 Centre for Vision Research, York University, Toronto, Canada2 Department of Psychology, York University, Toronto, Canada3 Department of Ophthalmology and Vision Sciences, University of Toronto, Canada4 The Hospital for Sick Children, Toronto, Canada5 Vision Science Research Program, Toronto Western Hospital, Toronto, Canada

Received 23 April 2007; accepted 14 June 2007

Abstract—What happens to vision in the remaining eye following the loss of vision in the fellow eye?Does the one-eyed individual have supernormal visual ability with the remaining eye in order to adaptand compensate for the loss of binocularity and the binocular depth cue, stereopsis? There are subtlechanges in visual function following the complete loss of one eye from unilateral enucleation. Losingbinocularity early in life results in a dissociation in form perception and motion processing: someaspects of visual spatial ability are enhanced, whereas motion processing and oculomotor behaviourappear to be adversely affected suggesting they are intrinsically linked to the presence of binocularityin early life. These differential effects may be due to a number of factors, including plasticity throughrecruitment of resources to the remaining eye; the absence of binocular inhibitory interactions; and/oryears of monocular practice after enucleation. Finally, despite this dissociation of spatial vision andmotion processing, research that has examined visual direction and performance on monocular tasksshows adaptive effects as a result of the loss of one eye. Practically speaking, one-eyed individualsmaintain perfectly normal lives and are not limited by their lack of binocularity.

Keywords: Enucleation; monocular deprivation; spatial vision; motion processing; visual direction.

INTRODUCTION

It is a popular belief that losing the ability to use one sensory system results ina ‘sharpening’ of the other remaining senses. For example, the typical laypersonmight hold the belief that a person who is completely blind will have more acutehearing than someone with full vision. This is an empirical question — are blind

!To whom correspondence should be addressed. E-mail: [email protected]

510 J. K. E. Steeves et al.

people more perceptive to barely audible sounds or are they able to hear a widerrange of frequencies than normally sighted individuals?

Looking at another sensory modality and using functional brain imaging, researchon visual ability in deaf individuals with hearing loss early in life has demonstratedcortical changes in functional activation for visual stimuli. Specifically, enhancedsensitivity in multimodal areas in early deaf individuals has been shown (Bavelieret al., 2001). This would suggest that losing hearing early in life has allowed foradaptive cortical reorganization. In a more recent paper, however, Bavelier andcolleagues (2006) note that the story is not completely straightforward — deafindividuals exhibit both enhanced and diminished visual ability that is selectiveto specific visual capacities compared to hearing controls. In short, enhancedvisual skills in deaf individuals is not widespread but rather, limited to those visualabilities that are attentionally demanding and that would normally benefit from aconvergence of sensory information from both the auditory and visual domains.

Consider the case of losing just one eye. A similar question can be asked; doesthe remaining eye compensate for the loss of binocularity and lead to enhancedvisual function with the remaining eye? Here we review human behavioural studiesof visual performance in individuals who have complete monocularity followingthe loss of one eye (unilateral enucleation). The majority of the research hasbeen done on individuals who have lost one eye early in life, during postnatalvisual development, but a few studies have examined the loss of one eye later inlife. It is important to note that unilateral enucleation is unique in that it resultsin the most complete form of deprivation because the brain has absolutely novisual input from that eye once the end organ has been removed. This is unlikeother forms of monocular visual deprivation such as cataract, strabismus, ptosisor anisometropia that leave some, frequently abnormal, visual input. Completemonocular deafferentation provides a unique human model for examining theconsequences of the loss of binocularity.

Do one-eyed individuals see better with the remaining eye? The answer is similarto the findings from Bavelier’s work on early deaf individuals, both ‘yes’ and ‘no’.Losing one eye leads to both enhanced and reduced visual function depending uponthe visual capacity that is being measured and also on the age of the individual at thetime of the loss. This dissociation in visual performance appears to lie in whetherone is measuring visual spatial ability or visual motion processing and oculomotorsystems. That is, some aspects of visual spatial ability appear to be enhanced by theloss of binocularity; however, motion processing and oculomotor behaviour appearto be intrinsically linked to normal binocularity.

Here, we review the findings of studies that have specifically examined the visualconsequences of unilateral enucleation, the complete loss of one eye, on spatialvision and motion systems as well as on visual direction and performance duringmonocular tasks. We also discuss the issue of what is the appropriate controlcomparison group and how best to test this group. Finally, we conclude with abrief overview of physiological mechanisms that could account for cortical changes

Vision with one eye 511

following deafferentation of one eye and could lead to either enhanced or impairedvisual function in the remaining eye. We begin with spatial vision, which on thewhole shows either enhanced or equivalent performance in one-eyed observerscompared to binocularly-intact controls.

SPATIAL VISION

All of the studies that have examined visual performance in one-eyed individualsand are described below and are outlined in Table 1A (spatial vision) and Table 1B(motion processing tasks). Nicholas et al. (1996) tested contrast sensitivity inunilaterally enucleated adults and found that they had higher contrast sensitivitythan controls viewing monocularly at 2, 4 and 8 c/deg. At 4 c/deg, those whowere enucleated at 13 months or earlier had a peak sensitivity that was on theorder of 3.5 times better than controls viewing with the better eye. Table 2 showsthe approximate improvement in performance of one-eyed individuals compared tocontrols for spatial vision tasks. Moreover, when the enucleated observers werecategorized by age at enucleation there was a developmental relationship — thosewho had been enucleated before two years of age had better contrast sensitivityat 4 c/deg than those enucleated much later in life and control observers viewingbinocularly. These differences in contrast sensitivity show a critical period suchthat earlier enucleation leads to larger improvement in contrast sensitivity. Thesefindings suggest that contrast sensitivity develops at different rates for differentspatial frequencies and, further, that there is a period in early postnatal visualdevelopment where removal of an eye is followed by an improvement in contrastsensitivity at some spatial frequencies.

In a similar vein, Reed et al. (1996) examined acuity for letters defined by low tohigh luminance contrast (Regan, 1988). Unilaterally enucleated observers showedbetter letter recognition than normally sighted controls viewing monocularly andstrabismic observers viewing with their better eye. At the lower contrasts, theone-eyed individuals had better acuity compared to controls by 41–60% (seeTable 2). Enucleated observers, however, had similar performance to controlsviewing binocularly (Reed et al., 1997). Similarly, González et al. (2002) testedacuity for luminance contrast-defined illiterate E optotypes, both centrally andperipherally (7" eccentricity). Consistent with the findings of Reed and colleagues(1996, 1997), for central viewing the enucleated observers demonstrated betteracuity at high and low contrast levels than controls viewing monocularly butcomparable acuity to that of controls viewing binocularly. With peripheral viewing,enucleated observers showed a small acuity difference in favour of the temporalhemifield. These one-eyed observers had better acuity than the better eye ofstrabismic observers (amblyopic or non-amblyopic) even though all groups hadcomparable foveal decimal acuity of 1.0 or better. Moreover, the enucleated grouphad better low contrast acuity, by approximately 95% (see Table 2) and similarhigh contrast acuity compared to the control group viewing monocularly. Because


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the temporal hemifield has been shown to develop earlier than the nasal hemifield(Lewis and Maurer, 1992) it is likely that early unilateral enucleation has a greatereffect on the earlier-developing nasal retina, to its benefit. This favourable effectmay be due to the complete absence of binocular competitive mechanisms duringits maturation thereby allowing the nasal retina a neural advantage and therefore,enhanced temporal field acuity.

Freeman and Bradley (1980) measured high contrast vernier acuity in adults withunilateral enucleation or unilateral amblyopia who had normal Snellen acuity in thefunctional or remaining eye. They found that the monocular individuals had highervernier acuities than binocularly normal observers tested monocularly. Their one-eyed individual had a vernier offset threshold that was 55% better than the mean ofcontrols viewing with the better eye (see Table 2 for a summary). This finding ofenhanced vernier acuity in monocular individuals, however, was not replicated inunilaterally enucleated children when vernier acuity was tested at a medium levelof contrast (González et al., 1992). Vernier acuity was also no different in thenon-deprived eye of an individual with unilateral cataract compared to the patient’sidentical twin (Johnson et al., 1982). Since vernier acuity is known to greatlyimprove with practice (McKee and Westheimer, 1978; Poggio et al., 1992) it ispossible that the findings of Freeman and Bradley are the result of using highlytrained monocular observers (optometry students) and relatively untrained controls.González and colleagues, however, demonstrated a significant effect of age attesting such that younger observers had poorer resolution than older observers.From these data, it appears that vernier acuity reaches adult levels at 8–9 years ofage and others have shown that it approaches adult levels at 5 years of age (Zankeret al., 1992). Similar findings were found by Schwartz et al. (1987) regarding ageat enucleation and vernier acuity.

Steeves et al. (2004) tested another form of hyperacuity in adult one-eyedobservers. They tested performance for global shape discrimination by measuringdiscrimination of small deviations from circularity using radial frequency patterns athigh and low contrast (Wilkinson et al., 1998). Control observers were tested in twomonocular conditions: (1) dichoptic viewing — a luminance-matched grey field wasshown to the non-viewing eye in an attempt to optimize monocular performance and(2) wearing a black eye patch over the non-viewing eye. Sensitivity to low-contrastglobal shape was equivalent in unilaterally enucleated observers and binocularly-viewing controls. However, both binocularly-viewing controls and enucleatedobservers showed superior performance compared to controls viewing in eithermonocular condition. While enhancement in performance was not as large as thatshown with contrast sensitivity or low contrast letter acuity, significant improvementrelative to controls on this task ranged from 2 to 11% (see Table 2).

At low contrast, the dichoptic control group was more sensitive than controlswearing the black eye patch, which suggests that dichoptic viewing is a superiormethod for testing controls monocularly. If differences in retinal illumination de-grade monocular performance for binocularly-intact controls, presenting a feature-


less field of equivalent brightness might be a better way of testing control observersmonocularly rather than using the traditional black eye patch, which lowers the illu-mination to the non-viewing eye. This is likely the case since hyperacuity thresholdsat low contrast were improved for the dichoptic compared to the eye patch monoc-ular control condition. It is remarkable that, nonetheless, the enucleated observersexhibited superior performance at low contrast compared to this dichoptic viewingcontrol group.

High-contrast second-order texture-defined letter detection and discrimination(Regan and Hong, 1994) was compared between enucleated observers and monocu-larly- and binocularly-viewing controls (Steeves et al., 2002). On this spatial vi-sion task, the enucleated observers showed no significant difference in performancecompared to controls, although the one-eyed observers did show a trend for betterdetection of texture-defined letters compared to monocularly-viewing controls. Itwould be worthwhile to measure low-contrast performance for this task since it re-quires somewhat higher-level spatial integration, being a second-order spatial task.

Recently, Troxler fading was measured in enucleated observers compared tocontrols (González et al., 2007). Time to fading for all observers was a functionof brightness contrast. It was significantly faster with monocular (i.e. patched) thanwith binocular viewing, for the controls. In contrast, one-eyed observers showedequivalent time to fading compared to binocular viewing controls. Moreover,they showed significantly longer fading times than the two-eyed observers viewingmonocularly, on the order of three times longer for low contrast stimuli (seeTable 2). A control experiment showed that these findings were not due toworse fixation stability, larger pupil sizes, or an unusually large blinking rate inthe enucleated group. Enucleated observers exhibited a slight miosis which, ifreplicated with a larger sample, would actually indicate that, rather than mimickingthe consensual pupilary response of closing one eye, the visual system opts insteadfor a larger depth of field and reduced optical aberrations for the remaining eye. Onewould expect, therefore, that the fading times of the enucleated observers would beshorter than those of the monocularly viewing controls because the retinal image is,in fact, dimmer and as a result, likely to fade faster. This, however, is not the case,suggesting differences between the groups at a cortical level.

To summarize the data from studies of spatial vision, visual ability of one-eyedobservers is by and large enhanced compared to two-eyed controls. This is mostoften the case for tests that have used low contrast stimuli. Enhanced visual abilityhas been demonstrated for detection tasks such as contrast sensitivity, letter acuityand for some hyperacuity tasks as well as for the phenomenon of Troxler fading.The findings from these studies are summarized in Tables 1A and 2. It is possiblethat binocular interactions in the controls may have little effect at higher contrastbut are more evident with low contrast stimuli. It is important to note that whenexperimenters attempted to minimize binocular interactions for the controls with theuse of dichoptic viewing, the enucleated observers nevertheless performed betterthan the controls. Enhanced spatial visual ability in one-eyed observers could be


due to the removal of inhibitory binocular interactions that are known to underliethe tuning of retinal disparity (Poggio et al., 1998) and binocular rivalry (Fox,1991). With respect to several of the lower contrast spatial vision tasks, enucleatedobservers indeed appear to have compensated for the loss of binocularity. These dataare opposite from the deficits in spatial vision that are seen with other forms of visualdeprivation such as cataract, strabismus, ptosis and anisometropia (e.g. Mansouriand Hess, 2006; McKee et al., 2003), suggesting that unilateral enucleation is a verydistinct form of monocular visual deprivation.

MOTION PROCESSING AND OCULOMOTOR SYSTEMS

While visual spatial ability tends to be enhanced with the loss of one eye, motionprocessing and oculomotor performance tends to be adversely affected by it. Motionprocessing has been examined in one-eyed observers on a number of different tasksand is summarized in Table 1B. Bowns et al. (1994) examined relative motiondiscrimination for shearing stimuli in the upper and lower visual field. Stimuliwere a textured surface with a discontinuity between the upper and lower fieldthat was defined by relative speed differences but moved in the same direction.They found that early enucleated adults and binocularly intact age-matched controlshave similar thresholds for detecting relative motion. These groups, however,exhibit opposite biases in the perceived velocity of stimuli in the upper and lowerhemifields. Controls were more likely to judge the upper hemifield as fasterwhile enucleated observers judged the bottom hemifield as faster. Bowns et al.hypothesized that if one-eyed observers or other subjects with weak stereopsisattempt to use motion parallax (a system used for far space) as a substitute forstereoscopic information (a system used for near space), a reversal of the normalvisual field bias (Previc, 1990; Skrandies, 1987) could occur.

In fact, González et al. (1989) measured depth perception in a test modified fromthe standard Howard Dolman depth perception test in which the only cue for depthwas motion parallax. One might expect that enucleated observers would be superiorin the use of monocular cues for depth, since depth from stereopsis is not availableto them. Surprisingly, one-eyed young children do not spontaneously make lateralmovements of the head when determining depth and as a result they show poorerdepth perception compared to controls. Subsequently, however, González andcolleagues instructed the children to move the head from side to side and re-tested their thresholds. In this case, depth perception from motion parallax inthese younger one-eyed observers was comparable to that of an older control groupviewing binocularly.

These findings stand in contrast with those of Marotta et al. (1995), who foundlarger and faster head movements in enucleated subjects in a reaching and graspingtask. It is important to note, however, that this discrepancy can be explained by thesignificant age difference in participants in the two studies — the subjects in thestudy by González et al. (1989) were young (mean age = 12 years) while those


in the paper by Marotta et al., were much older (mean age = 32.4 years). Further,Marotta and colleagues remarked that the proportion of self-generated lateral andvertical head movements versus forward head movements increases as a function ofpost-enucleation time, which is also consistent with the age differences between thetwo studies. It is likely that one-eyed individuals learn to increase the proportionof lateral and vertical head movements to make better use of motion parallaxwhile reducing forward head movements that produce less helpful informationfor estimating depth (Marotta et al., 1995; Simpson, 1993). Similar age-relatedfindings with depth perception in one-eyed observers were reported by Schwartzet al. (1987).

The use of the monocular motion-in-depth cue tau (! ), the angular rate of ex-pansion of a looming object (Hoyle, 1957), for the perception of time to contactwas measured in one-eyed observers by Steeves et al. (2000). Again, as with mo-tion parallax, this monocular cue for motion in depth might sometimes be useful ineveryday life since many objects have familiar sizes. Surprisingly, however, enu-cleated observers cannot estimate time to collision (TTC) of an approaching objectbased on this monocular cue better than the controls. In fact, the majority of one-eyed observers were worse, showing larger errors in estimating TTC than controlsviewing monocularly. Interestingly, most one-eyed individuals relied on other task-irrelevant variables such as the stimulus’ starting size. Such variables, although notrelevant to this task, would be useful in the real world where objects have familiarsizes. This study provides evidence that one-eyed observers learn to use as manyoptical variables as possible to compensate for the lack of binocular information.

The ability of one-eyed observers to recognize letters defined by second ordermotion — the relative motion of elements within the boundary of the letter to thatof elements in the background (Regan and Hong, 1990) — is also significantlypoorer than binocularly viewing controls (Steeves et al., 2002). When compared tomonocularly viewing controls, their performance is equivalent but shows a trend forpoorer recognition. Developmental data have shown that sensitivity to form-from-motion contrast has a longer developmental time course than that for luminancecontrast (Giaschi and Regan, 1997). Together with the developmental evidence,the data from one-eyed observers suggest that the loss of binocularity early in lifeis operating on two distinct processing mechanisms (spatial vision versus motionprocessing) and as a result affects them differentially.

Other findings with respect to motion processing and oculomotor performancedemonstrate that, unlike spatial vision, these systems are adversely affected by theloss of binocularity. Poor motion processing is consistent with data from subjectswith deficient stereopsis (see Tychsen, 1993, for a review). Steeves et al. (2002)examined left–right direction discrimination in a motion coherence task. Whilebinocularly intact controls showed no asymmetry in direction discrimination, theenucleated group showed significantly higher temporalward than nasalward motioncoherence thresholds. Moreover, this nasalward bias was absent in the subjectwho had undergone enucleation at the oldest age (43 months). All other one-eyed


observers were enucleated before 36 months of age, suggesting a critical period forthe role of binocularity in the development of horizontal motion discrimination.

This perceptual asymmetry in direction discrimination is consistent with both sen-sorimotor and cortical motion processing asymmetries that have been demonstratedin early enucleated observers by others. For example, Reed et al. (1991) measuredoptokinetic nystagmus (OKN) in early unilaterally enucleated observers and foundthat 63% had small but significant asymmetries of OKN, favouring nasally-directedmotion in the visual field. Day (1995) compared OKN and motion visual evokedpotentials (mVEPs) to horizontally moving vertical sinusoidal gratings in differentmonocular populations. Day found that 25% of observers with early enucleationhad asymmetrical OKN and further that 17% of observers showed no optokineticresponse at all. Higher motion VEP asymmetries were seen in enucleated observerswho lost the eye at a young age compared to those who had lost vision as an adult orto those who were congenitally monocular. These sensorimotor and cortical motionasymmetries reflect a critical period that has been demonstrated for the developmentof symmetrical motion processing in young infants. For instance, normal human in-fants tend to show more OKN to motion that is moving nasally than temporallywhen viewing moving stimuli monocularly (Atkinson and Braddick, 1981; Naegleand Held, 1982) and develop more symmetrical OKN (similar to that of an adult) ataround 5 to 6 months of age (Naegle and Held, 1982). Similarly, Norcia et al. (1991)examined mVEPs to horizontally moving vertical sinusoidal gratings in young in-fants from 2 to 26 weeks of age compared to normal adults. They also found di-rectional asymmetries in favour of nasally-directed stimuli. This evidence suggeststhat the maturation of cortical mechanisms is involved in the development of sym-metrical motion responses and that there is a critical period for normal maturation.

VISUAL DIRECTION AND PERFORMANCE ON MONOCULAR TASKS

We have two eyes yet experience a singular view of the world — the signals fromthe two eyes are integrated and projected to this ‘egocentre’ without the observer’shaving any conscious eye of origin information (Steinbach et al., 1985). What doesthe one-eyed observer experience, since the only viewing eye is displaced laterallywith respect to the midline of the body? Do they adapt the egocentre accordingly?While developing the laws of visual direction Hering (1942/1879) predicted that theorigin of visual direction, or egocenter, would shift towards the remaining eye, if oneeye was lost. Moidell et al. (1988) measured the position of the midline relative tothe remaining eye in children with one eye. Children were asked to align a non-visible rod, using their hands, with a visible ‘fireman’s hose’ that was aligned to thevisual axis of the remaining eye. Binocular children with one eye covered, alignedthe rod with their midline. The one-eyed children (five years of age and older),however, aligned the rod close to the position of the remaining eye (approximately75% of the distance between the midline and the remaining eye), suggesting thatthe midline was plastic and had shifted toward the ‘visual’ centre relative to the


body. In this study, children were enucleated up to four years of age and there wasno relationship to egocentre position and age at enucleation. This suggests that theegocentre is plastic at least up to four years of age. To test this hypothesis, healthybinocular adults were monocularly patched for a one month period, and showedvirtually no change in egocentre location (Dengis et al., 1992). Further, adultswho underwent monocular enucleation after a lifetime of normal binocular visionshow limited plasticity in egocentre location (unpublished observations, Dengis andSteinbach).

Barbeito (1983) confirmed a clinical observation that young children will placea tube between their two eyes when asked to look through it at a target. Hefound this ‘cyclops’ effect in children aged 3–4 years. How do age and visualexperience play a role in the ‘cyclops effect’, since most adults can use a tubefor sighting by effortlessly placing it over one eye? Dengis and colleagues (1993)used the ‘look through a tube’ technique in three groups — binocularly normal;unilaterally enucleated; and strabismic children. They found that the egocentre wasessentially built-in and children in all groups sighted with the tube midway betweenthe two eyes. This effect was present in the youngest children who could be tested(1.1 years). Interestingly, the presence of normal binocular experience was notnecessary for the cyclops response. For all groups, the ‘cyclops effect’ diminishedas they grew older and children sighted monocularly by about four years of age.

Using different types of tubes for sighting, Dengis et al. (1996) examined theemergence of monocular sighting as it develops from the ‘cyclops effect’. Childrenprogress through a series of behavioral stages that ultimately lead to the adultperformance, which is monocular sighting with the non-sighting eye closed andthe head straight.

Turning the head, or ‘face turn’ as it is sometimes called in the clinical literature,frequently occurs in one-eyed children (Goltz et al., 1997). Head turn almost alwaysoccurred with the head turned so as to bring the remaining eye closer to the midlineof the body. This head turn also has the beneficial effect of reducing occlusionof the visual field by the nose. Others have described a head turn in the oppositedirection in five patients with esotropia following unilateral enucleation (Helvestonet al., 1985). Unlike the one-eyed observers in the study by Goltz et al. (1997) whoshowed no nystagmus, these patients had esotropia and the presence of an abductionnystagmus with an extreme adduction null point (a position of the eye in the orbitwhere the nystagmus dampens).

Every monocular task we perform includes immediate feedback about its success.If we try to look through a microscope, we know from tactile and visual feedbackwhether or not the preferred eye is aligned with the eye piece. What happens inthe absence of this feedback? Dengis et al. (1998) instructed adults and childrento monocularly sight through a tube but they had placed a liquid–crystal shutterdirectly in front of the subject’s face. As soon as the subject initiated the movementof the tube toward the eye, the shutter became opaque, thereby preventing any visualfeedback. At the same time, the glass plate of the shutter also prevented any tactile


feedback about where on the face the tube might have touched. The results weresurprising: the tube was placed at the midline by adults and children with normalbinocular visual development as well as by those with strabismus. The enucleatedsubjects, on the other hand, all placed the tube over their remaining eye. This findingsuggests that binocular observers (both normal and strabismic) revert to egocentresighting in the absence of visual and tactile feedback but that the egocentre shift inone-eyed observers has truly been re-wired toward the remaining eye.

These results suggest that our orienting responses, when moving ourselvesthrough space, use the midline egocentre as the origin from which we judgedirection (Ono and Mapp, 1995; Ono et al., 2002). Only when we are forced intoa monocular task, and have feedback about how we perform that task, do we use alearned pattern of responses developed with a preferred eye. It would be worthwhileto study orienting behaviour in one-eyed observers using more natural tasks — thiswas tried in the past with some success (Dengis et al., 1995; González et al., 1999),showing better accuracy in one-eyed observers consistent with a shift in egocentretoward the remaining eye.

POSSIBLE MECHANISMS OF VISUAL PLASTICITY FOLLOWINGENUCLEATION

At least three kinds of processes may lie behind the dissociation in visual perfor-mance of enucleated observers in spatial vision and motion processing systems,some of which have been mentioned above. These are: (a) plasticity through re-cruitment by the remaining eye of the resources normally assigned to the missingeye, (b) the absence of binocular inhibitory interactions resulting from the removalof one eye and (c) monocular practice over the years after enucleation.

Plasticity

The visual system has been shown to exhibit a remarkable plasticity in response tovisual deprivation in animals (see reviews in Daw, 1995; Fox and Wong, 2005;Karmarkar and Dan, 2006; Kiorpes and Movshon, 2003; Krahe et al., 2005).Specifically, various physiological changes have been demonstrated in animalsfollowing unilateral enucleation, many of which suggest that the remaining eyemay make use of the deafferented cells to its advantage. This has been calledrecruitment, since visually driven brain cells driven normally by the enucleated eyemay have been ‘recruited’ by the remaining eye. There is evidence of recruitmentafter deprivation, which increases the cortical space innervated by the remainingeye. Cells dominated partially or completely by one eye undergo a reorganizationafter lack of visual input and become primarily responsive to the other eye (Gilbertand Wiesel, 1992; Hubel and Wiesel, 1962; Hubel et al., 1977; Kratz and Spear,1976). In addition, monocular enucleation reduces apoptosis in ganglion cells in theremaining eye and preserves or even expands their central connections (Guillery,


1989). This reorganization can occur within hours, depending on the nature ofthe lesion (Schmid et al., 1995) and can involve other sensory modalities (Kahnand Krubitzer, 2002; Kujala et al., 2000). One study has shown physiologicalevidence in humans for cortical reorganization following unilateral enucleationduring infancy for tumour. Horton and Hocking (1998a) showed a lack ofocular dominance columns in the striate cortex of children with early monocularenucleation.

Binocular competition that is required for normal formation of the visual systemdoes not necessarily require visual experience, since competition for corticalspace and synaptic formation may begin before birth. For example, monocularenucleation that takes place prenatally rather than postnatally appears to producemore significant changes in the functional properties of cortical neurons in favourof the remaining eye. Prenatally enucleated macaque monkeys show an absenceof ocular dominance columns (Rakic, 1981). Prenatally enucleated ferrets showa disruption in the formation of the fibres in the uncrossed pathways (Taylorand Guillery, 1995). In short, competition between the two eyes for synapticspace is necessary for the normal formation of the visual pathways and thisoperates at both cortical and subcortical levels. Although the animal results arecomplex and extrapolation to humans is made difficult by both empirical andtechnical considerations, the anatomical and physiological changes found in non-human species as a result of enucleation or deprivation and changes in binocularcompetition suggest the possibility of psychophysical correlates in humans.

On one hand, the deficits in motion processing in one-eyed observers thatwere outlined earlier may be accounted for by an interruption in binocularityduring a postnatal sensitive period. In order to establish symmetrical motionprocessing, normal levels of binocularity, in particular binocular competition, maybe required during development of its neural substrates. Other cases of binocularinterruption or an imbalance in binocular competition in early visual developmentshow asymmetrical motion processing. For example, OKN is asymmetrical inchildren and adults with strabismus with an onset before two years of age (e.g.Atkinson and Braddick, 1981; Reed et al., 1991; Steeves et al., 1999). In thecase of unilateral enucleation, it appears that removing an eye at an early age haslead to an imbalance in (or rather, a complete absence of) the normal binocularcompetitive interactions that are necessary for the establishment of symmetricalmotion perception. On the other hand, the enhancement in spatial vision that isseen in one-eyed observers can also be explained by the anatomical consequencesof changes in binocular competition. Factors other than recruitment could also playa role in enhancing spatial processing including an absence of binocular interactionsand monocular practice.

Absence of inhibitory binocular interactions

Neurons in primary and secondary cortical visual areas are binocular and exhibitan intracortical system of inhibitory interactions. Nicholas et al. (1996) found that


the peak contrast sensitivity at 4 c/deg of early-enucleated subjects was greater thanthe binocular performance of controls by a factor greater than

#2, the theoretical

limit attainable if all the cortical cells were driven by the remaining eye (Campbelland Green, 1965). The authors proposed that the enucleated subjects’ performancemay be enhanced by the removal of the inhibitory binocular interactions, which areknown to underlie the tuning to retinal disparity (Poggio et al., 1998) and binocularrivalry (Fox, 1991; Mueller, 1990). A reduction in horizontal connections forbinocular vision in V1 has been observed in naturally strabismic monkeys (Tychsenet al., 2004). The removal, by enucleation, of this intracortical inhibitory systemmay make individual neurons more sensitive to contrast.

In addition, it is also likely that the performance of normally binocular subjectsunder monocular viewing conditions may be adversely affected by the binocularrivalry that is produced by an eye patch, which is commonly used for such tests. Al-though this view contradicts Levelt’s (1965a, 1965b) proposition that a contourlessstimulus cannot suppress a patterned one and should remain suppressed indefinitely,it has received ample support from a number of studies (see González et al., 2007;Howard, 2002, for reviews). The rivalry from the occluded eye does not exhibit theclassic temporal and spatial features of rivalry from a textured field, and althoughbinocularly normal observers exhibit very few changes in a variety of visual func-tions after a month of monocular patching (Dengis et al., 1992), they report frequentand annoying blackouts during occlusion which is very likely a consequence of therivalry from the patched eye.

Even when visual disturbances are either not perceived or reported by observers,the type of monocular occlusion used has distinctive effects on binocular perfor-mance, including acuity (Horowitz, 1949) and contrast sensitivity and acuity (Wild-soet et al., 1998). Binocular acuity and contrast sensitivity deteriorate as a functionof interocular illuminance differences, and increasing the density of the filter in frontof one eye eventually leads to binocular inhibition (i.e. binocular viewing becomesworse than monocular viewing). That the perceived brightness of a target can belower when one eye is covered by a neutral density filter than when the filtered eyeis closed, is a phenomenon called Fechner’s paradox (Fechner, 1860/1966).

The absence of inhibitory binocular interactions in the enucleated group mayexplain in part their resistance to fading (González et al., 2007) and their superiorperformance in other contrast-defined tasks, but does not rule out the effectsof plasticity through recruitment and imbalanced binocular competition. In thediscrimination of radial frequency patterns, Steeves et al. (2004) found that despitethe superiority of dichoptic over patched viewing for the controls, performancewas still not equivalent to that with binocular viewing or to that of the enucleatedobservers. This finding may reflect the consequences of recruitment and plasticityafter enucleation that has been observed anatomically in humans by Horton andHocking (1998a).

Plasticity after enucleation is not limited to an immature visual system, however.Klaeger-Manzanell et al. (1994) reported a two-step recovery of visual function in


an amblyopic adult whose acuity in the amblyopic eye improved after vision loss inthe fixing eye. After remaining stable for 13 months, there was a further increase inacuity after the formerly better eye was enucleated. Improvements in visual functionin the amblyopic eye after a reduction of visual function in the non-amblyopic eyehave been documented in adults by others (Hamid et al., 1991; Romero-Apis et al.,1982) and are consistent with data from animals (Harwerth et al., 1986; Horton andHocking, 1998b; Prusky et al., 2006; Smith, 1982).

Finally, the superior monocular sensitivity for spatial vision of one-eyed observerscould also be predicted by a model involving simple cortical pooling and a “winner-take-all-rule” as proposed by McKee et al. (2003). This model can explain someof the enucleated data showing better spatial sensitivity but fails to predict thediminished acuity of non-amblyopic and amblyopic strabismic observers using theirpreferred eye. This suggests that complete deafferentation with enucleation has avery distinct operation on the visual system when compared to non-deafferentingforms of monocular deprivation.

Monocular practice

Even though monocular practice may be an important component of the superiorvisual spatial performance of enucleated observers, González et al. (1998) foundthat age at enucleation rather than years since enucleation is a better predictor ofvisual performance. When comparing two early (under 2 years of age) and one late(in adulthood) enucleated patient with two normal controls viewing monocularly,the early enucleated observers had better improvement in performance with practicefor recognition of motion-defined letters. In fact, the learning rate of the earlyenucleated observers was higher than that of the controls and the late enucleatedsubject. Similarly, other studies have also seen more plasticity in early compared tolate enucleated observers (Nicholas et al., 1996).

The data described here highlight the problems in studying the effects of binoculardeprivation and the difficulties in selecting appropriate control groups for one-eyedobservers. On one hand, while strabismic amblyopia, anisometropia, and unilateralcataracts all involve monocular deprivation, they also involve abnormal binocularinteractions which result in inferior performance in many visual functions. On theother hand, in binocularly normal observers, patching or closing one eye does notproduce ‘monocular’ vision but rather a condition of weak binocular rivalry which,in addition to probability and neural summation explains the superiority of theirbinocular over monocular, that is, patched-viewing (Howard, 2002).

In the study of visual plasticity and visual development, one-eyed observers pro-vide us with a useful model to study the roles of binocularity in visual processing.Further, this monocular model leads to very different effects compared to othermodels of ‘monocular’ deprivation. Complete monocular deafferentation, particu-larly when it occurs early in life, results in a divergence of two visual subsystems.The evidence suggests that spatial vision and motion systems are distinct visualsubsystems that are differentially affected by the loss of an eye early in life. While


spatial vision appears somewhat enhanced following the loss of one eye, motionprocessing and oculomotor systems are poorer. Motion processing and oculomotorfunction must require balanced binocular input to establish these systems. Finally,despite the dissociation that is seen in these visual subsystems, one-eyed individualsmaintain perfectly normal lives and are not limited by their lack of binocularity.

Acknowledgements

We are grateful to Linda Lillakas for her comments and editorial assistance. Supportfor this review comes from the Natural Sciences and Engineering Research Council,The Sir Jules Thorn Charitable Trust, The Krembil Family Foundation, AtkinsonFaculty and the Vision Sciences Research Program at the Toronto Western Hospital.

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Vision with one eye: a review of visual function following unilateral enucleation

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