Monocular spatial distortion in strabismic...

Volume 20Number 2 Reports 263

Seattle. This research was supported in part by NEIgrant 1 R01 EY 02510 to Ronald G. Boothe, NIH re-search grants RR 00166 to the Regional Primate Center,NICHD 02274 to the Washington Regional Child De-velopment and Mental Retardation Center, and EY01730 to the Interdisciplinary Ophthalmic and VisionResearch Center of the Department of Ophthalmology.Part of this work was presented at the spring meeting ofthe Association for Research in Vision and Ophthalmol-ogy, Sarasota, Fla., 1980. Submitted for publication July24, 1980. Reprint requests: Lynne Kiorpes, Infant Pri-mate Laboratory, WJ-10, University of Washington,Seattle, Wash. 98195.

Key words: strabismus, monkeys, animal model

REFERENCES1. Duke-Elder S and Wybar D: System of Ophthal-

mology. Vol. VI. Ocular motility and strabismus.London, 1973, Henry Kimpton.

2. von Noorden G: Burian and von Noorden's Binocu-lar Vision and Ocular Motility: Theory and Man-agement of Strabismus. St. Louis, 1980, The C. V.Mosby Co.

3. von Noorden G and Dowling J: Behavioral studies instrabismic amblyopia. Arch Ophthalmol 84:215,1970.

4. Jampolsky A: Unequal visual inputs and strabismusmanagement: a comparison of human and animalstrabismus. In Symposium on Strabismus, Transac-tions of the New Orleans Academy of Ophthalmol-ogy. St. Louis, 1978, The C. V. Mosby Co.

5. Polyak S: The Vertebrate Visual System. Chicago,1957, University of Chicago Press.

6. Skavenski A A, Robinson DA, Steinman RM, andTimberlake GT: Miniature eye movements of fixa-tion in rhesus monkey. Vision Res 15:1269, 1975.

7. Ruppenthal GC: Nursery Care of Nonhuman Pri-mates. New York, 1979, Plenum Press, chap. 13.

8. Regal DM, Boothe RG, Teller DY, and Sackett GP:Visual acuity and visual responsiveness in dark-reared monkeys (Macaca nemestrina). Vision Res.16:523, 1976.

9. Kiorpes L and Boothe RG: The time course for thedevelopment of strabismic amblyopia in infant mon-keys (Macaca nemestrina). Invest Ophthalmol VisSci 19:841, 1980.

10. Teller DY and Boothe RG: Development of vision ininfant primates. Trans Ophthalmol Soc UK 99:333,1979.

Monocular spatial distortion in strabismicamblyopia. HAROLD E. BEDELL* AND MER-

TON C. FLOM.*

We examined monocular spatial vision of strabismicamblyopes by measuring errors of relative directional-

ization (specifying whether or not two targets are in ver-tical alignment) and partitioning (equating left- andright-field spaces). Abnormally large errors were madewhen fixation occurred with the amblyopic eye; theseerrors are not attributable to reduced acuity, unsteadyfixation, or eccentric fixation. From the results we inferthat monocular space perception of strabismic amblyopiceyes is severely distorted and is characterized by "bend-ing" of vertical lines of direction and by local "com-pressions" and "expansions" of horizontal spatial values.Such distortions can readily account for many of theoculomotor abnormalities of the amblyopic eye as well asfor the strabismic subject's phenomenological descriptionof the difficulties experienced in using this eye—difficulties that are typically much worse than the re-duced acuity would- predict.

In their classic paper, Wald and Burian1 pro-posed that the visual deficit of strabismic ambly-opic eyes affects form or pattern vision with spar-ing of light perception and spatial projection. Inorder to assess form vision, Wald and Burian mea-sured visual acuity for letters presented on a stan-dard clinical chart. Pirennes2 subsequent analysisof visual acuity (resolution) as a special type oflight difference discrimination raises doubt asto whether such visual acuity measurementsadequately evaluate form vision.

A number of observations indicate that the vi-sual deficit in strabismic amblyopia is not ade-quately specified in terms of acuity (or of gratingcontrast sensitivity, which has recently been pro-posed to supplant traditional visual acuity mea-sures3 but which is also readily subsumed byPirennes light-difference discrimination analysis).Measured visual acuity of amblyopic eyes typicallyshows considerable variability and depends, inpart, on whether a full chart, single lines of letters,or isolated symbols are used.4 Hess et al.5 havepresented contrast sensitivity curves for two stra-bismic amblyopic eyes that are indistinguishablefrom those for their subjects' preferred eyes. In-deed, grating resolution thresholds reported forstrabismic amblyopic eyes are typically much bet-ter than expected from the performance of theseeyes on letter acuity tests.3 Clearly, the visualangle subtended by an acuity or grating target maynot be the sole variable, or even the most rele-vant, in determining the visual performance of anamblyopic eye.

About 20 years ago, Pugh6' 7 reported that am-blyopes perceived distortions when they viewedtest letters with the affected eye; their descriptionsincluded abnormal spacing between letters or theirparts, fragmenting of letter, and changes in theshapes of letters. Recently, Hess et al.5 reported

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264 Reports Invest. Ophtfialnwl. Vis. Sci.February 1981

Table I. Partitioning results for the amblyopiceye of Subject T. M. with the central rodimaged approximately at the fovea

Fig. 1. Stimulus configuration used to evaluaterelative directionalization; it shows the test linedisplaced leftward of center of the hourglass-shaped fiducial target. When fixating with theamblyopic eye, many of our strabismic subjectscalled a test line displaced from center by aboutthis amount "right" and "left" equally often.

similar descriptions of distortions from amblyopesviewing suprathreshold bar gratings. Quantifica-tion of this spatial distortion was probably first ac-complished by Schor.8 He performed partitioningexperiments on one strabismic amblyope, the af-fected eye showing relative underestimations ofdistances in the temporal field by as much as afactor of 3.

We present here for several strabismic ambly-opic eyes measures of (1) spatial distortion, quan-tified as the relative overestimations and under-estimations of spaces in the nasal and temporalfields and (2) aberrated relative directionalization,quantified as the lateral offset of a target for it to beperceived as vertically aligned with two others. Incombination, spatial distortion and directionaliza-tion errors are probably sufficiently large to accountfor many of the visual deficits of amblyopic eyes.We therefore propose that the Wald-Burian earlyconcept of impaired form vision be broadened to

Standardspace, right

of fovea(deg)

0.51.02.03.04.05.06.08.0

Subjectively equiv-alent space, left

of fovea(deg ± 1 S.D.)

0.56 ± 0.081.33 d3.20 d3.81 d4.86 d5.72 j6.42 i8.53 j

t 0.16b 0.28t 0.28t 0.44= 0t 0.04= 0.12

Standard spaceEquivalent space

0.890.750.630.790.820.870.930.94

impaired spatial vision and that measures of spatialerrors be used to specify and describe this majorvisual deficit of strabismic amblyopia.

Methods. We tested monocular relative direc-tionalization and partitioning of space with visualtargets presented on the screen of a CommodorePET microcomputer and viewed from a distance of50 cm. The nonviewing eye was occluded with anopaque patch and padded shut.

To measure monocular relative directionaliza-tion, subjects specified the perceived horizontallocation of a luminous vertical line (3.4 by 32 minarc) with respect to the vertical axis of an hour-glass-shaped fiducial target. This target (Fig. 1)consisted of two luminous isosceles triangles (base4.6 deg, altitude 2.8 deg) with the altitudes alignedvertically and the facing apices separated by 1.6deg. The test line was flashed for 130 msec at oneof several horizontal locations rightward or left-ward of the vertical axis of the fiducial target. Toencourage fixation at the center of the target andto ready the subject for the test line presentation,two vertical lines (7 by 32 min arc; one at the tip ofeach triangle) were flashed for two half-sec-on andhalf-sec-off cycles before flashing of the test line.

For monocular partitioning of space, subjectsfixated the central one of three horizontally sepa-rated luminous vertical lines (3.4 by 32 min arc).The position of the righthand line was fixed anddefined a standard space between it and the cen-tral fixation line. For each fixed position of therighthand standard target, the subject adjustedthe lefthand line (in 3 min arc steps) to produce aspace between it and the fixation line that wasperceptually equal to the standard space.

ResultsRelative directionalization. The results for our

13 strabismic amblyopes were plotted as the per-centage of "right," "left," and "centered" re-



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LEFT 50 40 30 20 10 0 10 20 30 40 50 RIGHTDISPLACEMENT OF LINE FROM CENTER (MIN)

Fig. 2. Relative directionalization data for two strabismic amblyopic eyes are plotted as thepercentages of "right" (triangles), "left" (squares), and "centered" (circles) responses for eachof several displacements of a test line from the center of the fiducial target. The locus ofsubjective alignment is the crossing point of the "right" and "left" response functions. Thelocus of subjective alignment is about 30 min left of center for the left amblyopic eye of subjectR. W. (40A esotropia and 8A hypertropia of the left eye; left eye acuity 20/80 with 2A nasaleccentric fixation) and about 18 min left of center for the left amblyopic eye of subject J. F. (20A

esotropia of the left eye; left eye acuity 20/180 with 2A temporal and 0.8A inferior eccentricfixation).

sponses for each of the several positions of the testline relative to the center of the fiducial target.The plots for two of these subjects are shown inFig. 2. We define the locus of subjective alignmentas the position of the test line at which the per-centages of "right" and "left" responses are equal(indicated where the curves cross). For 11 of our13 amblyopes the locus of subjective alignmentwas displaced from the physical center of thefiducial target by 10 to 40 min arc in the amblyopiceye. In contrast, the locus of subjective alignmentfor normal eyes (Fig. 3, a) and our amblyopes'preferred eyes was never more than 1.5 min arcaway from the physical center of the fiducialtarget.* Thus errors of relative directionalizationfor the amblyopic eyes were about 10-fold largerthan the greatest errors found in the preferredeyes or in either eye of nonamblyopic subjects.

To what extent can these measured errors ofrelative directionalization be attributed to the re-

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*The normal threshold for detecting misalignment of atest line from a fiducial, which is the typical dependentvariable in relative directionalization studies, is on theorder of 5 to 20 sec arc. That the locus of subjectivealignment for some of our normal subjects was displacedfrom the fiducial by over 1 min arc is explained by ourdependent variable, which is a measure of constant errorrather than threshold, as well as by our spatial and tem-poral stimulus parameters, which are not optimal forrelative directionalization judgments.9

LEFT 30 20 10 0 10 20 30 RIGHT

DISPLACEMENT OF LINE FROM CENTER (MIN)

Fig. 3. a, Locus of subjective alignment for theright eye of normal subject G. S. is almost exactlycentered, b, When foveally fixating 3 deg left ofthe fiducial target, G.S.'s locus of subjectivealignment is displaced about 15 min leftward, i.e.,in the direction of the foveal axis, c, Locus of sub-jective alignment is close to center for the righteye of subject B. A., despite a congenital jerk nys-tagmus having an amplitude of about 3 deg and afrequency of about 3 Hz. Visual acuity of B.A.'sright eye is 20/70.


266 Reports Invest. Ophtlwlmol. Vis. Sci.February 1981

IS

i I I I I 1

0.6

PREFERRED RIGHT EYE

A) 0 2 4 6 8 0 2

STANDARD SPACE (DEC RIGHT FIELD)

STANDARD SPACE (DEC RIGHT FIELD)

Figs. 4a and 4b. Monocular partition settings (± 1 S.D.) of two strabismic amblyopes (T. M.and J. F.) are plotted as the size of the space in the left field (ordinate) that was judgedequivalent to a standard space in the right field (abscissa). Shown above is the ratio of thestandard to the equivalent space for each standard space matched. The settings for the twoamblyopic eyes reveal marked and nonuniform spatial asymmetries; settings for the preferredeyes are much closer to physical matches (indicated by the dashed lines both above and below).Subject T. M. has 15A esotropia of the left eye; its acuity is 20/100 with 3A of nasal eccentricfixation; the clinical data for Subject J. F. are given in the legend to Fig. 2.



duced acuity or to the unsteady, eccentric fixationof amblyopic eyes? In persons with congenital nys-tagmus, wherein there is reduced acuity and veryunstable fixation, we found the locus of subjectivealignment to be close to the physical center of thefiducial target (Fig. 3, c). The effect of eccentricfixation was examined by having normal subjectsmonocularly view the stimulus array eccentrically;under this condition, normal subjects made rela-tive directionalization errors similar in magnitudeto some of the amblyopes, but opposite in direc-tion (Fig. 3, b). Although the locus of subjectivealignment for eccentrically viewing normal sub-jects was shifted from the fiducial target towardthe foveal axis, for the majority of the amblyopiceyes (eight of the 11 who made errors of 10 min arcor larger) it was shifted away from the foveal axisand lay on the opposite side of the fiducial target.We conclude that the errors of relative direc-tionalization for strabismic amblyopic eyes are notaccounted for by their reduced acuity or their un-steady and eccentric fixation. Indeed, the use of anextrafoveal retinal location for fixation by theamblyopic eye might diminish the magnitude ofthe measured relative directionalization error—byan amount equal to the oppositely directed errormade by a normal eye viewing the stimulus eccen-trically.

Partitioning in the horizontal meridian. In ourpartitioning procedure we always presented thestandard space to the right of the fixation mark,and the subject adjusted the lefthand target so thatthe space between it and the fixation mark wasperceived equal to the standard space. We de-picted the obtained results with the size of thestandard space plotted on the abscissa and the sub-ject's target setting (for subjectively equivalentspace) plotted on the ordinate.

The most common response for the six ambly-opic eyes we tested is shown for two subjects inFigs. 4a and 4b. For the largest standard space of 8deg, both subjects set the lefthand target onlyabout 7 deg from fixation to perceive the twospaces equal. Since both subjects had amblyopia ofthe left eye, the smaller setting was in the tem-poral field, indicating a relative overestimation ofthis space in this field. For the smallest standardspace of 0.5 deg, the subjects set the temporalfield target between 1 and 2 deg, indicating under-estimation of this space. The course of the datapoints between 8 and 0.5 deg indicates a transitionfrom overestimation to underestimation at about 2to 3 deg. In this region of transition the flatness ofthe "curve" suggests that several standard spacesin the nasal field were perceived as a single size (or

nearly so), which was therefore matched with asingle target setting (or nearly so) in the temporalfield.

Can these marked nasal-temporal asymmetriesbe explained by the fixational unsteadiness and/orimaging of the central target at a nonfoveal locusthat occurs with eccentric fixation? Subjects withcongenital nystagmus did not exhibit large parti-tioning errors, indicating that the retinal imagemotion generated by fixational unsteadiness prob-ably was not responsible for the partitioning errorsof amblyopic eyes. With regard to the retinal locusissue, we performed experiments on one oi ouramblyopes in which the central rod was imaged ator very close to the fovea; with the standard andtest spaces on opposite sides of the fovea, markedspatial asymmetries were still evident (Table I).

We have shown marked spatial asymmetrieswith amblyopic-eye fixation at the eccentric locusand at the fovea. However, we cannot tell whetherthe distortion of monocular space indicated bythese asymmetries is confined to one side of thefixing point or whether it is present on both sides.To clarify this point, we directed two subjects(T. M. and J. F.) to fixate first the rightmost andthen the leftmost target and to adjust the positionof the lefthand target to define two perceptuallyequal spaces first within the temporal, then withinthe nasal field. Abnormally large partitioning er-rors were made within both half fields, indicatingthat distortion of space was present on both sidesof the eccentric fixation locus and extended to atleast the fovea, perhaps somewhat beyond it.

Discussion. Monocular testing of the affectedeye of strabismic amblyopes revealed large con-stant errors in the relative directionalization ofvertically arranged targets and marked asymme-tries in the partitioning of horizontal spaces. Webelieve that these spatial errors, occurring inorthogonally separate meridians, represent twomanifestations of a single deficit—namely, a se-vere distortion of monocular perceived spacewithin at least the central field of these amblyopiceyes. The errors made with the amblyopic eyefixating indicate a distortion of perceived spacecharacterized by "bending" of vertical lines, eachhaving a common visual direction, and by local"expansions" and "compressions" of spatial valuesacross the field.

Is such distortion of perceived monocular spacean unexpected finding in strabismic amblyopiceyes? When the preferred eye of a strabismicamblyope is occluded as a therapeutic measure,the patient often reports distortion, especially ofreading material. An associated complaint is the


268 Reports Invest. Ophthalmol. Vis. Sci.February 1981

inability to move the amblyopic eye accuratelyfrom one word to another. Indeed, the inaccurateeye movements that amblyopes often describe,and which have been verified objectively,8 canreadily be appreciated to be a consequence of dis-torted space perception. Hence, aspects of un-steady fixation, irregular smooth pursuit, and di-rectional overshooting and undershooting of sac-cades, all of which characterize the oculomotorbehavior of strabismic amblyopic eyes,8 becomeexplicable in terms of the aberrated visual errorsignals that must result when the directionaliza-tion of a stimulus in space is subject to markednonuniform distortion.

This spatial distortion must also have deleteriousconsequences for visual acuity. Relative "expan-sion" and "compression" of space as well as "bend-ing" of vertical lines of direction must be expectedto distort the features of single optotypes6 and,when presented in an array, to blend neighboringletters together into invalid or unrecognizable per-cepts.7 As a result of the amblyopic eye's unsteadyfixation, these percepts must also be considered tobe changing in time.5 Distortion would be expectedto have a severe effect on the identification of com-plex targets, such as optotypes. In contrast, thereshould be a much less disturbing influence on thedetection of repetitive spatial patterns such as grat-ings, for which the positions of the individual ele-ments (spatial phase) are relatively unimportant.Thus the typical finding that visual acuity forstrabismic amblyopic eyes is poorer for letters thanfor gratings2 is understandable because distortionof monocular space limits performance on the lettertask whereas performance on the grating task isprimarily determined by the resolving propertiesof the visual system. Indeed, the visual complaintsof strabismic subjects when viewing with theamblyopic eye are more readily attributable toaberration of monocular space sense than to im-pairment of the resolving capacity of the visualsystem.

Hence, unlike Pugh,6> 7 we do not view theseaberrations of monocular spatial vision as merelyan interesting but isolated phenomenon associatedwith amblyopic vision. Nor do we agree with Pughthat these spatial aberrations represent abnor-malities at the level of the retina. The magnitudeof the spatial errors as well as their probableamelioration with successful therapy suggest to us,as to Hess et al.,5 that these errors occur centrallyand probably at the visual cortex. Whatever theiranatomical and physiological substrate, only quan-titative analysis of these monocular spatial distor-tions can reveal the extent to which they account

for or underlie the sensory and oculomotor ab-normalities of strabismic amblyopic eyes.

From the School of Optometry, University of Cali-fornia, Berkeley. Supported by National Eye InstituteResearch Grants EY 02125 and EY 03694 (Dr. Flom).Submitted for publication July 8, 1980. Reprint requests:Harold E. Bedell, Ph.D., College of Optometry, Uni-versity of Houston, Central Campus, Houston, Texas77004. *Present address: College of Optometry, Uni-versity of Houston, Houston, Texas.

Key words: strabismus, amblyopia, space perception,partitioning errors, directionalization, acuity, eyemovements

REFERENCES1. Wald G and Burian HM: The dissociation of form

vision and light perception in strabismic amblyopia.Am J Ophthalmol 27:950, 1944.

2. Pirenne MH: Visual acuity. In The Eye, Vol. 2, Dav-son, H, editor. New York, 1962, Academic Press,Inc., pp. 175-195.

3. Hess RF: On the relationship between strabismicamblyopia and eccentric fixation. Br J Ophthalmol61:767, 1977.

4. Irvine SR: Amblyopia ex anopsia. Observations onretinal inhibition, scotoma, projection, light differ-ence discrimination and visual acuity. Trans AmOphthalmol Soc 46:527, 1948.

5. Hess RF, Campbell FW, and Greenhalgh T: On thenature of the neural abnormality in human ambly-opia; neural aberrations and neural sensitivity loss.Pfliigers Arch 377:201, 1978.

6. Pugh M: Visual distortion in amblyopia. Br J Oph-thalmol 42:449, 1958.

7. Pugh M: Amblyopia and the retina. Br J Ophthalmol46:193, 1962.

8. Schor CM: Oculomotor and neurosensory analysis ofamblyopia. Doctoral dissertation, University of Cali-fornia, Berkeley, 1972.

9. French JW: The unaided eye. Part III. Trans Opt Soc(London) 21:127, 1920.

Normal square wave jerks. YUVAL O.HERISHANU AND JAMES A. SHARPE.

Fixation stability of the saccadic system was investigatedby infrared reflection oculography in 29 normal subjects,young and elderly. Square wave jerks consisting of spon-taneous horizontal saccadic excursions of 0.5° and over,followed some 200 msec later by corrective saccades,were recorded in 24% of subjects. The frequency ofsquare wave jerks in the elderly was significantly higherthan in young subjects. The results suggest that squarewave jerks more frequent than 9/min in young patientscan be considered abnormal.

Square wave jerks (SWJ) are sporadic horizon-tal conjugate saccades away from the intended po-

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