Abnormal saccadic substitution duringsmall-amplitude pursuit tracking

in amblyopic eyesKenneth J. Ciuffreda, Robert V. Kenyon, and Lawrence Stark

Small-amplitude, low-velocity, predictable triangular tracking ivas tested in patients havingamblyopia without strabismus, intermittent strabismus, or constant strabismus amblyopia bymeans of a photoelectric eye-movement recording technique. In the majority of amblyopicpatients, abnormal saccadic substitution was found; that is, abnornudly large saccades ratherthan small-amplitude smooth movements were used by the amblyopic eye to follow a spotstimulus that moved horizontally with low to high frequencies. Pursuit for the same range ofstimuli was normal for binocular tracking and for monocular tracking with the dominant eye,pointing to a sensory rather than motor basis for the defect. This abnormal saccadic substitu-tion response appeared to be related to the presence of amblyopia rather than strabismus.Several possible mechanisms responsible for causing this unusual response are discussed,including impairment of direction sense over small central regions of the amblyopic eye.

Key words: amblyopia, pursuit movements, saccadic movements,abnormal direction sense, suppression, strabismus,

eye movements

D,uring tracking of a smoothly movingtarget, the pursuit system attempts to matcheye velocity with target velocity and therebystabilize the target image on the retina. Ac-cumulated position errors between the targetand central retina are corrected by the sac-cadic system, which places the image of thetarget within the sensitive central foveal re-gion.1- 2 Thus the end result of accurate track-

From the School of Optometry, University of California,Berkeley.

This work was supported in part by NIH Training GrantEY 00076 (K.J.C. and R.V.K.) and an Auxiliary to theAmerican Optometric Association Research Fellow-ship (K.J.C).

Submitted for publication May 12, 1978.Reprint requests: Dr. Kenneth J. Ciuffreda, Depart-

ment of Basic Optometric Sciences, State College ofOptometry, State University of New York, 100 East24th St., New York, N. Y. 10010.

ing is a relatively stabilized image of the mov-ing target on the fovea.

Pursuit performance has been investigatedin patients having amblyopia and strabismusby means of objective eye-movement record-ing techniques. Von Noorden and Macken-sen3 found tracking of large-amplitude, si-nusoidally moving stimuli to be impaired attarget frequencies beyond approximately 0.5and 0.3 Hz in the normal and amblyopiceyes, respectively, of strabismic amblyopes.Fukai et al.4 found pursuit abnormalitiesfor tracking of large-amplitude, sinusoidallymoving stimuli in the amblyopic and domi-nant eyes in many patients having amblyopia(with or without strabismus). Marked direc-tional impairment of pursuit for targets (6 de-grees peak-to-peak amplitude) moving intothe nasal retina of amblyopic eyes in patientshaving constant strabismus amblyopia has re-cently been reported.5

506 0146-0404/79/050506+ll$01.10/0 © 1979 Assoc. for Res. in Vis. and Ophthal., Inc.

Volume 18Number 5 Abnormal saccadic substitution, amblyopic eyes 507

We expanded on previous investigationsby using small-amplitude stimuli, extendingthe range of stimulus frequencies used, andincluding patients from three clinically im-portant diagnostic groups. In our study, pur-suit movements in patients having amblyopiawithout strabismus, intermittent strabismus,or constant strabismus amblyopia were test-ed. Binocular tracking, as well as monoculartracking with the amblyopic or the dominanteye, were evaluated. Our new finding wasabnormal saccadic substitution during small-amplitude pursuit tracking in amblyopiceyes; that is, abnormally large saccadesrather than small-amplitude smooth move-ments were used to track the target.

Methods

A photoelectric method was used to recordhorizontal eye position.6 The bandwidth of theentire recording system was 75 Hz (—3 dB). Aheadrest and chinrest, as well as a bite bar in mostcases, were used to stabilize the head. Eye move-ments were analyzed directly from strip chartrecords.

A minicomputer (PDP-8/I) was used to gen-erate a constant velocity (triangular) stimulus inthe horizontal meridian having amplitudes of 1, 2,4, and 8 degrees and velocities of 0.95, 1.75, 2.25,3.75, and 6.75 degrees/sec (corresponding to fre-quencies of 0.48, 0.89, 1.12, 1.88, and 3.38 Hz,respectively), in any possible amplitude-velocitycombination. All combinations were not tested oneach patient. The small target (6 min arc) con-sisted of a bright spot of light viewed by the sub-ject on a display screen placed either 57 or 91 cmaway on the midline. Target luminance was alwaysmaintained at least 1 log unit above backgroundscreen luminance. Mean smooth-pursuit gain wasdetermined by averaging values of smooth-pursuitgain (eye velocity divided by target velocity) foreach individual segment of (smooth) tracking for 5to 15 cycles of target motion.

Twelve patients were obtained from either thegeneral refraction clinic or the orthoptics clinic atthe optometry school. Ages ranged from 15 to 33years, with a mean age of 25.5. All patients had athorough vision examination and were free of ocu-lar or neurological disease. Only functional ambly-opes were used in the study. Patients from threediagnostic groups were included: (1) amblyopiawithout strabismus, (2) intermittent strabismus

(with or without mild amblyopia), and (3) constantstrabismus amblyopia. We classified patients ac-cording to the presence of amblyopia and/orstrabismus. This classification has proved success-ful for us in terms of relating eye movement ab-normalities in our patients to either amblyopia orstrabismus.7"13 We are aware of two otherclassifications of amblyopia,14- l5 both based on theclinical condition (i.e., strabismus or anisomet-ropia) believed responsible for producing theamblyopia. We believe that all three classificationsprovide important, but different, ways of ap-proaching and understanding underlying mecha-nisms and abnormalities related to amblyopia andstrabismus. Spectacle or contact lens prescriptionwas worn during all testing. See Table I for com-plete clinical data.

During monocular tracking, the eye not beingtested either was tightly covered by a full, blackpatch and black tape or was occluded by a large,black partition blocking the target and most of theroom from that eyes view. Method of occlusiondid not have any effect on eye movements.

Results

The results of small-amplitude trackingwith the amblyopic eye clearly demonstratedthat patients from each diagnostic groupprimarily used saccades rather than smoothmovements to follow the target (Fig. 1, a toc). Moreover, the amplitudes of these track-ing saccades were generally two to five timeslarger than the target amplitude. Thus sub-stitution of small-amplitude smooth move-ments by abnormally large saccades occurredduring small-amplitude, constant-velocitytracking with the amblyopic eye in responseto both nasalward and templeward targetmotions on the retina. This abnormal saccadicsubstitution was not found during binoculartracking or monocular tracking with the dom-inant eye (Fig. 2) in any patient. Mean pur-suit gain in the dominant eye generallyranged from 0.7 to 0.95. These values forpredictable triangular tracking with the dom-inant eye compare well to those values foundunder the same test conditions in our labora-tory for normal (nonamblyopic) control sub-jects. Moreover, these values compare wellto those reported by Puckett and Steinman16

(0.6 to 0.9) for tracking 3-degree randomized

508 Ciuffreda, Kenyon, and Stark Invest. Ophthalmol. Visual Sri.May 1979

Table I. Clinical data of patients and presence of abnormal saccadic substitutionin amblyopic (or nondominant) eye

Patient Age PrescriptionVisualacuity

Vergenceabnormality

(prism diopters)Eccentric fixation(prism diopters)

Constant strabismus amblyopia:1

2

3

4

5

25

23

15

32

33

LE + 2.00 = -0.25 x 130RE + 2.25LE + 3.75 = -0.50 x 165RE + 0.50LE - 1.50RE - 1.75LE + 4.00RE pianoLE + 0.75 = -0.50 x 40RE + 0.25 =0.50 x 180

Amblyopia without strabismus:6

7

8

24

25

19

LE + 0.75 = -2.00 x 90RE pi = -0.50 x 19LE - 2.50 = -1.25 x 172RE - 5.00 = -0.75 x 5LE + 5.00RE + 3.00

Intermittent strabismus with or without mild amblyopia9

10

11

12

22

31

32

25

LE - 0.75 = -0.25 x 148RE - 3.00 = -0.25 x 100LE - 5.00RE - 4.50 = -0.75 x 20LE + 0.75 = -1.75 x 180RE + 1.25 = -3.50 x 5

LE pianoRE - 1.00

20/2520/1520/3020/1520/12220/2020/27720/2020/63020/10

20/3820/2020/2520/4020/11020/15

20/2020/2020/2020/2020/2020/23

20/3220/16

1-2 ET LE

18 ET LE

10 ET LE and1 HTLE

4 ETLE

5-6 ET LE and2 HTLE

None

None

None

18 ALT. XT and12 HT LE

15 XT LE

40-50 XT RE

10 XT LE and20 HT LE

1/2 nasal LE

1 nasal LE

2.5 nasal and 2 su-perior LE

16 nasal and 4 su-perior LE

2.5-3.5 nasal and3-4 superior LE

2 nasal and 2 in-ferior LE

2 nasal and 2 in-ferior RE

2 temporal LE

Slight unsteadycentral LE, RE

Central steadyLE, RE

1 nasal andsuperiorRE

1/2 nasal LE

single ramps having velocities of 1 and 2degrees/sec. Although abnormal saccadicsubstitution rarely occurred for tracking oflarger target amplitudes (4 and 8 degrees)in these patients (Fig. 3), other pursuit ab-normalities found included saccadic intru-sions7' n (see Discussion for description),marked variability of pursuit gain,7 and in-frequent marked directional smooth-pursuitgain asymmetry7 (high gain (>0.7) smoothpursuit in one direction and primarily sac-cadic tracking in the opposite direction). Ab-normal saccadic substitution, if found in apatient, was almost always (~95% of thetime) present for 1-degree target amplitudes,generally present (~85% of the time) for2-degree target amplitudes, and infrequentlypresent (<5% of the time) for 4- or 8-degreetarget amplitudes. It was present for the fullrange of low, moderate, and high target fre-quencies used (see Methods). Mean pursuit

gain for tracking of 4- and 8-degreeamplitudes with the amblyopic eye generallyranged from 0.4 to 0.7. No direct relationshipbetween depth of amblyopia and degree oftracking anomaly was evident, although ab-normal saccadic substitution was alwaysfound in moderate and deep amblyopes.

Abnormal saccadic substitution was foundduring monocular tracking with the ambly-opic eye in one of three patients having am-blyopia without strabismus (see Table I). Arepresentative record is presented in Fig. 1,a. Following the initial brief period when thepatient appeared not to be trying to track thetarget, large saccades having amplitudes upto 2.5 degrees (middle of trace) and small sac-cades having amplitudes of approximately 1.0degree were used to track the target. Littleevidence of smooth movements was presentin the tracking records.

Abnormal saccadic substitution was found

Volume 18Number 5 Abnormal saccadic substitution, amblyopic eyes 509

Presence of abnormalsaccadic substitution

Amblyopia therapy orcorrective surgery

No

Yes

Yes

Yes

Yes

No

No

Yes

No

No

Yes

No

Surgery, age 16

Surgery, age 6

No

No

Surgery, age 6

No

No

Amblyopia therapybefore & duringstudy

No

Surgery, age 16

Therapy initiated 1month before study

No

during monocular tracking with the ambly-opic eye in four of five patients having con-stant strabismus amblyopia (see Table I). Arepresentative record for Patient 4 is pre-sented in Fig. 1, b. Evident was a markedabsence of smooth movements. Tracking oc-curred primarily by large saccades (up to 5degrees in amplitude). These large trackingsaccades were initiated approximately 350 to900 msec following a change in target direc-tion. Similar results were found for the otherthree patients.

Abnormal saccadic substitution was foundduring monocular tracking with the ambly-opic eye in one of two patients having inter-mittent strabismus with mild amblyopia.Neither of two patients having intermittentstrabismus without amblyopia exhibited thisphenomenon (see Table I). A representativerecord for Patient 11 is shown in Fig. 1, c.Tracking with the amblyopic eye was per-

formed primarily by abnormally large sac-cades (up to 5 degrees in amplitude). How-ever, at target turnaround points, there wassome evidence of smooth tracking (withsmooth pursuit gain as high as 0.7 for brief300 msec periods).

Discussion

Abnormal saccadic substitution was foundin the majority of amblyopic eyes duringsmall-amplitude, constant-velocity trackingfor a variety of low (~0.5 Hz), moderate(-1.0 Hz), and high (-2.0 Hz) target fre-quencies. It is interesting that saccadic sub-stitution commonly occurs in normal subjectsduring high-frequency tracking of smoothlymoving targets; however, saccadic ampli-tudes are typically less than or equal to targetamplitude.6 That predictive mechanisms6

exerted little influence during tracking wassuggested by two general findings. (1) Thelarge tracking saccades generally occurred atleast 200 msec following a change in targetdirection; the presence of tracking saccadesinitiated up to 900 msec following a change intarget direction is consistent with recent re-ports of increased saccadic latencies in am-blyopic eyes.9' 10 (2) The eye lagged behindthe target when smooth movements werepresent.

Does abnormal saccadic substitution ap-pear to be related primarily to the presenceof amblyopia or strabismus? Two lines of evi-dence suggest it is the former. (1) Patient 8having amblyopia without strabismus ex-hibited abnormal saccadic substitution. (2)Our two patients having intermittent stra-bismus without amblyopia did not displaythis anomalous tracking response. Thesefindings suggest that amblyopia and notstrabismus is the primary common factor.Only Patient 11 represents a possible excep-tion to our conclusion. However, this patientappears to us to represent a borderline case.With Patient 11 having eccentric fixation of 1prism diopter, visual acuity of 20/23, and in-creased saccadic latencies as frequently asfound in more typical amblyopic patients,9- 10

we believe that placement into an "ambly-opic" classification is justified, even though

510 Ciuffreda, Kenyon, and StarkInvest, Ophthalmol. Visual Sci,

May 1979

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OT 4

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Fig. 1. Monocular tracking with the amblyopic eye. Top traces are eye positions, and bottomtraces are stimuli. T and N near calibration bars indicate templeward and nasalward move-ments of eye, respectively. A, Patient 8: amblyopic eye 20/110; amblyopia without strabismus.Stimulus is 1.0 degree amplitude, 3.75 degrees/sec velocity, 1.88 Hz. Abnormally large sac-cades (up to 2.5 degrees in amplitude) and some small saccades (<1 degree in amplitude) usedto track target. Little evidence of smooth tracking found. B, Patient 4: amblyopic eye 20/277;constant strabismus amblyopia. Stimulus is 1.0 degree amplitude, 0.95 degrees/sec velocity,0.48 Hz. Little evidence of smooth following movements found; instead, target tracked byabnormally large saccades (up to 5.0 degrees in amplitude). C, Patient 11: mildly amblyopiceye 20/23; intermittent strabismus. Stimulus is 1.0 degree amplitude, 2.25 degrees/sec veloc-ity, 1.12 Hz. Abnormally large saccades (up to 5 degrees in amplitude), rather than smoothmovements, generally used to track target. Some short periods of smooth tracking found atturnaround points. Results of these patients clearly shows similarity of abnormal trackingresponse across the three diagnostic groups, as well as lack of dependence between targetfrequency (with constant amplitude) and abnormal tracking response.

visual acuity was not 20/30 or worse, and thedifference in acuity between the eyes was nottwo lines or greater, two common clinicalcriteria for specification of amblyopia.17

Does abnormal saccadic substitution rep-resent a true tracking response, or is it simplya threshold phenomenon in which "ambly-

opic fixation tremor" occurs until target mo-tion is large enough to elicit smooth pursuitresponses? Our evidence suggests the formeris true. Fixational and tracking eye move-ments were recorded and studied in our pa-tients and reported in detail elsewhere.7"13

Several interesting and important abnor-

Volume 18Number 5 Abnormal saccadic substitution, amblyopic eyes 511

o* 4°[MiiJ.

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Fig. 2. Eye position as a function of time for dominant eye (20/15) of Patient 8 havingamblyopia without strabismus. In each pair of records, upper trace is eye position, and lowertrace is stimulus. Target amplitudes are 1 degree (upper left), 2 degrees (upper right), and4 degrees (lower trace). T and N near calibration bars indicate templeward and nasalwardmovement of the eye, respectively. No evidence of abnormal saccadic substitution present,and pursuit gain within normal limits. Compare upper left trace of this figure to trace in Fig. 1,A, for Patient 8 tracking same target with amblyopic eye.

malities were noted, and some are presentedin Figs. 4 and 5. The first abnormality is sac-cadic intrusions (a pair of saccades of approx-imately equal amplitude (average ~1.0 de-gree) but of opposite direction); they occurirregularly during fixation but average ap-proximately 1/sec and have intersaccadic in-tervals ranging from 150 to 500 msec) (Fig. 4,upper left). These saccadic intrusions duringfixation are quite different from the abnormalsaccadic substitution response found in ouramblyopes (Fig. 4, upper right). During ab-normal saccadic substitution, regular move-ments (generally 2 to 5 degrees in amplitude)occur ~95% of the time in the same directionas target motion, and these are only foundwhen patients attempt to track the small-amplitude stimulus. Thus abnormal saccadicsubstitution clearly represents a definite and

purposeful tracking response on the part ofthe patient to follow a moving stimulus (all pa-tients did perceive the target as moving fromside to side) and is not simply the occurrenceof large, irregularly timed fixational saccades(saccadic intrusions). Furthermore, althoughthe saccades of the abnormal saccadic sub-stitution pattern occurred to either side of apreviously established baseline position, inmany instances saccadic intrusions duringfixation were directed nasally in these samepatients.n The second abnormality, increaseddrift amplitude7 (up to 3.5 degrees peak topeak) and velocity12 (up to 3.3 degrees/sec)(Fig. 4, lower left), resulted in relativelysmooth, "saccade-free" traces, and this clear-ly represents a fixation response quite differ-ent from the abnormal saccadic substitutiontracking response. The third abnormality is

512 Ciuffreda, Kenyon, and Stark Invest. Ophthaltnol. Visual Sd,May 1979

1-1

• " ! _

- - J

- 1

-7

1Fig. 3. Eye position as a function of time for amblyopic eye of Patient 8 having amblyopiawithout strabismus. Each set of traces show eye velocity, eye position, and stimulus, respec-tively, from top to bottom. Target amplitudes are 1 degree (upper left), 2 degrees (upperright), 4 degrees (lower left), and 8 degrees (lower right). T and N near calibration bars indicatetenipleward and nasalward movement of the eye, respectively. Abnormal saccadic substitutionclearly seen for 1- and 2-degree stimuli, as well as some smooth movements at turnaroundpoints; for 4-degree stimulus, saccadic pursuit evident with over-all tracking responseamplitude being larger than stimulus amplitude; for 8-degree stimulus, saccadic pursuit evi-dent, but over-all tracking response amplitude approximately equal to stimulus amplitude.Thus, as target amplitude increases (but with constant velocity maintained), pursuit becomesmore normal-looking.

hypermetria. This was evidenced by singlelarge saccades (Fig. 4, lower right) and staticovershooting18 (Fig. 5) during small-amplitude step tracking. These two findingssuggest an increase in saccadic gain in theamblyopic eye for tracking of small targetdisplacements over the central retina. Thegain increase also provides a possible explana-tion, at least in part, for the large saccadesfound in our patients during predictablesmall-amplitude, constant-velocity tracking,i.e., the abnormal saccadic substitution re-sponse. That these abnormally large saccadesfrequently occurred 500 msec or more follow-ing a (predictable) target step change canbe explained by the increased saccadic la-

tencies found in the amblyopic eyes of thesetwo patients as is true for most amblyopiceyes.9' 10

Although there is no clear mechanism toexplain the phenomenon of abnormal sac-cadic substitution, we would like to discussthree possibilities. The first is abnormal di-rection sense in amblyopic eyes. As a result ofamblyopia, a depression of the directional-sensitivity gradient over the central retinamay occur. This could result in impairedand/or marked variability of direction sense,including errors or biases in estimation of an-gular distance of targets relative to the pre-ferred fixation locus. In the present situation,overestimation of small-angle target move-

Volume 18Nttmi?er 5 Abnormal saccadic substitution, amblyopic eyes 513

7LE

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- . . . • i(BfcL_

I HI

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Fig. 4. Fixation and tracking responses for amblyopic eye of Patient 4 having constant strabis-mus amblyopia (20/277). In each set of records, upper trace is amblyopic eye position, andlower trace is stimulus. Upper left, Midline fixation showing intermittent steadiness of eye aswell as some saccadic intrusions. Note irregularity and relatively small amplitude of intrusions.Upper right, Abnormal saccadic substitution in response to small-amplitude (2 degrees),constant-velocity (0.95 degrees/sec, 1.12 Hz) stimulus. Note regularity and large amplitudes ofsaccadic movements during abnormal saccadic substitution in contrast to irregularity and smallamplitudes of saccadic intrusions during fixation (Upper left). Also note similarity betweenabnormal saccadic substitution shown here and response of same patient tracking stimulushaving different amplitude (1 degree) and frequency (0.48 Hz) but same velocity (0.95degrees/sec) (Fig. 1, B), suggesting generalized nature of response. Lower left, Fixation traceshowing period of increased amblyopic drift7 and only a few irregularly occurring small sac-cades. Thus both this trace and Upper left trace show fixation characteristics that are clearlymuch different from abnormal saccadic substitution tracking response (Upper right). Lowerright, Predictable (0.5 Hz), small-amplitude (0.6 degrees) step tracking. Note some largesaccades (up to 9.0 degrees in amplitude) in response to periodic target changes, suggestingfluctuations of saccadic gain, especially greater than 1.0. Increased saccadic gains noted forboth abnormal saccadic substitution (Upper right) and step tracking suggest similar underlyingmechanism operating in response to small-amplitude changes in retinal stimulation inamblyopic eye.

ments on the retina would result in the inap-propriately large eye movements exhibitedby our patients. If our abnormal-direction-sense hypothesis is correct and is generalizedfor all types of tracking, one would predictthat hypermetria (static overshooting18 andsingle large saccades) would be commonlyfound during small-amplitude step tracking;

although hypermetria was found in ambly-opes (Figs. 4 and 5), it was not as consistent afinding as was abnormal saccadic substitution.However, it appears reasonable to assumethat a constantly moving target providing re-peated information regarding target directionby stimulating retinal regions in an orderlysequence would elicit this response in a more

514 Ciuffreda, Kenyon, and StarkInvest. Ophthahnol. Visual. Sci.

May 1979

| 3 SEC—|

Fig. 5. Predictable, small-amplitude step tracking response in former amblyopic eye of Patient8 (similar to that found in same patient when visual acuity was 20/11012). Upper trace is eyeposition, and lower trace is stimulus (0.5 Hz, 0.6 degree amplitude). Note static overshootspresent in majority of responses, suggesting increased gain of saccadic eye movement systemfor small changes in target position. This saccadic gain increase appears to be related toincreased saccadic amplitudes observed in abnormal saccadic substitution responses (Fig. 4,Upper right) and the large saccades sometimes observed in Patient 4 during small-amplitudestep tracking (Fig. 4, Lower right).

consistent manner than would a target whichmoves in relatively infrequent, discrete, ran-dom steps and only stimulates small, isolatedretinal regions. Our idea of abnormal direc-tion sense in amblyopic eyes is in agreementwith that of previous investigators. Macken-sen19 believed that the physiological su-periority of the fovea and the graded sensoryfunction of the macula region had been trans-formed, due to amblyopia, into a region ofequivalent sensory characteristics; Macken-sen20 also believed that eccentric fixation rep-resented a transposition of the principal vi-sual direction; von Noorden21 believed thatamblyopes possessed a vagueness of direc-tional sense; and Griffin17 believed directionsense in an amblyopic eye with eccentricfixation is impaired and results in past-pointing. These factors could contribute tothe anomalous tracking response found in ourpatients. It is interesting to speculate that ournobon of abnormal direction sense in ambly-opic eyes, based upon dynamic test results,may be related to eccentric fixation, which isbased upon static test results. Eccentric fixa-tion is found in the majority of amblyopiceyes,22' 23 and its presence suggests a shift in

the zero sensorimotor directional referencepoint under "steady-state" monocular testconditions. A second mechanism, possiblyrelated to the first, is suppression. It is awell-established fact that suppression iscommonly found in amblyopic eyes underbinocular test conditions.24' 25 Suppressionmay result in an over-all reduction in sen-sitivity over central retinal regions of theamblyopic eye. This sensorially depressedcentral zone would correspond to all or partof the area undergoing suppression in theamblyopic eye during binocular viewing. Ifthis is true, a strategy of placing the targetjust outside this depressed region might beadopted during monocular tracking with theamblyopic eye. Impaired or vague directionsense would prevent the phenomenon of ec-centric viewing from being reported. Thusthe average size of these large tracking sac-cades (—2.5 degrees) may represent the hori-zontal angular dimension of this abnormalregion. Direction, amplitude, and velocity oftarget movement could be processed for alonger period of time as target amplitude in-creased (and target movement on the retinaincreased). This could provide a possible ex-

Volume 18Number 5 Abnormal saccadic substitution, amblyopic eyes 515

planation for the abnormal tracking response(large tracking saccades and absence ofsmooth movements) found for small-targetexcursions and the more normal tracking re-sponse (lack of large tracking saccades andpresence of smooth movements) for larger-target excursions. This would be consistentwith the notion of increased information-processing delays in amblyopic eyes.9'10> 26~30

A third explanation might simply be that ab-normal saccadic substitution represents anormal phenomenon for small-amplitudepursuit tracking with the peripheral retina.However, the persistence of this abnormalresponse in one subject whose fixation cen-tralized during orthoptics therapy does notlend support to this idea.I2 Moreover, recentfindings by Fukai and Tsutsui31 suggest thatnonfoveal tracking would result in asymmet-ric pursuit rather than the symmetric abnor-mal saccadic substitution found in our pa-tients. That tracking small-amplitude stimulibinocularly or monocularly with the domi-nant eye never resulted in abnormal saccadicsubstitution further points to a sensory ratherthan motor basis for this pursuit defect.

The fact that all amblyopic patients withina diagnostic group, as well as across groupshaving similar visual acuities, did not exhibitabnormal saccadic substitution may be at-tributed to such factors as differences in ageof onset or constancy of the anomaly, sincethese factors are related to the period ofhuman vision development.32"40 Moreover,effects due primarily to suppression, com-monly found in strabismus with approxi-mately equal refractive error, may differ fromeffects due primarily to mild form depriva-tion, as found in anisometropia. Further test-ing of sensory and motor function over thecentral region of amblyopic eyes will be re-quired to elucidate possible interrelation-ships and common underlying mechanismsrelated to this pursuit defect.

REFERENCES1. Rashbass, C.: The relationship between saccadic and

smooth tracking eye movements, J. Physiol. 159:326, 1961.

2. Young, L.R., and Stark, L.: Variable feedback ex-periments testing a sampled data model for eye

tracking movements, IEEE Trans. Hum. FactorsElectronics, HFE-4:38, 1963.

3. von Noorden, G.K., and Mackensen, G.: Pursuitmovements of normal and amblyopic eyes: anelectro-ophthalmographic study. II. Pursuit move-ments in amblyopic eyes, Am. J. Ophthalmol.53:325, 1962.

4. Fukai, S., Tsutsui, J., and Nakamura, Y.: Abnormalpursuit movements of the fellow eye in amblyopiawith strabismus. In Moore, S., Mein, J., and Stock-bridge, L., editors: Orthoptics: Past, Present, Fu-ture, New York, 1976, Stratton IntercontinentalMedical Book Corp.

5. Schor, C M . : A directional impairment of eyemovement control in strabismus amblyopia, INVEST.OPHTHALMOL. 14:692, 1975.

6. Stark, L., Vossius, G., and Young, L.R.: Predictivecontrol of eye tracking movements, IRE Trans.Hum. Factors Electronics, HFE-3:52, 1962.

7. Ciuffreda, K.J.: Eye movements in amblyopia andstrabismus, Ph.D. dissertation, School of Op-tometry, University of California, Berkeley, 1977.

8. Kenyon, R. V.: Vergence eye movements in ambly-opia and strabismus, Ph.D. dissertation, School ofOptometry, University of California, Berkeley,1978.

9. Ciuffreda, K.J., Kenyon, R.V., and Stark, L.: In-creased saccadic latencies in amblyopic eyes, IN-VEST. OPHTHALMOL. VISUAL SCI. 17:697, 1978.

10. Ciuffreda, K.J., Kenyon, R.V., and Stark, L.: Pro-cessing delays in amblyopic eyes: evidence fromsaccadic latencies, Am. J. Optom. Physiol. Opt.55:187, 1978.

11. Ciuffreda, K.J., Kenyon, R.V., and Stark, L.: Sac-cadic intrusions in strabismus, Arch. Ophthalmol.(in press)

12. Ciuffreda, K.J., Kenyon, R.V., and Stark, L.: Dif-ferent rates of functional recover)' of eye movementsduring orthoptics treatment in an adult amblyope,INVEST. OPHTHALMOL. VISUAL SCI. 18:213, 1979.

13. Ciuffreda, K.J., Kenyon, R.V., and Stark, L.:Suppression of fixational saccades in strabismicand anisometropic amblyopia, Ophthalmic Res. (inpress).

14. von Noorden, G.K.: Classification of amblyopia,Am. J. Ophthalmol. 63:238, 1967.

15. Amos, J. F.: Refractive amblyopia: its classification,etiology, and epidemiology, J. Am. Optom. Assoc.48:489, 1977.

16. Puckett, J.W., and Steinman, R.M.: Tracking eyemovements with and without saccadic correction,Vision Res. 9:695, 1969.

17. Griffin, J.R.: Binocular Anomalies: Procedures forVision Therapy, Chicago, 1976, Professional PressInc., pp. 74-75, 95-96.

18. Bahill, A.T., Clark, M.R., and Stark, L.: Dynamicovershoot in saccadic movements is caused by neu-rological control signal reversals, Exp. Neurol.48:107, 1975.

19. Mackensen, G.: Blickbewegungen amblyopischerAugen, Graefes Archiv. Ophthalmol. 159:212, 1957.

516 Ciuffreda, Kenyon, and Stark Invest. Ophthalmol. Visual Sci.May 1979

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