Saccadic Intrusions in StrabismusKenneth J. Ciuffreda, OD, PhD; Robert V. Kenyon, PhD; Lawrence Stark, MD

\s=b\Fixational eye movements were stud-ied to determine the presence of and toquantify saccadic intrusions under mon-ocular and binocular viewing conditionsin subjects with intermittent strabismus,amblyopia without strabismus, or con-stant strabismus amblyopia. Saccadicintrusions were present under most testconditions in intermittent strabismus,were rarely observed in amblyopia withoutstrabismus, and were prominent duringmonocular fixation with the amblyopic eyein constant strabismus amblyopia. Thissuggests that the presence of saccadicintrusions was related to strabismus andnot amblyopia. There was no relationshipbetween saccadic intrusion amplitudeand visual acuity. Two possible mecha-nisms for producing intrusions are abnor-mally rapid regional visual adaptation andstrabismus-induced fixation degradation.

(Arch Ophthalmol 97:1673-1679, 1979)

Qaccadic intrusions refer to fast to-and-fro horizontal eye movements

observed in some patients, especiallyduring fixation.1 -' An intrusion con¬sists of an error-producing saccadefollowed 150 to 500 ms later by anerror-correcting saccade. Intrusionshave amplitudes generally rangingfrom 0.5° to 3.0° and occur one tofour times per second. While saccadicintrusions are frequently found inpatients with neurologic disorders,28

they are occasionally observed innormal subjects (unpublished observa¬tions).

Saccadic intrusions have also beenfound during monocular fixation withthe amblyopic eye in patients withstrabismus amblyopia. Intrusions areevident in the fixation records pre¬sented by Mackensen" and by vonNoorden and Mackensen10; saccadicintrusions and large single saccadeswere also found by von Noorden andBurian,11 and more recently by Hess,12during monocular fixation with theamblyopic eye. Schor and Flom13found median fixational saccadic am¬

plitude correlated with visual acuity inthe amblyopic eye of strabismicamblyopes.

We expanded on previous studies byinvestigating fixational eye move¬ments under both monocular and bin¬ocular test conditions, and by testingpatients with a wide range of visualacuities in three clinically importantand separable diagnostic groups: in¬termittent strabismus, amblyopiawithout strabismus, and constantstrabismus amblyopia. We hoped thatwe might provide an indication of thecause and functional importance ofsaccadic intrusions by extending our

study to include subjects with eitherintermittent strabismus or amblyopiawithout strabismus, both being diag¬nostic groups previously unstudied ina systematic manner.

METHODSHorizontal eye movements were meas¬

ured by a photoelectric technique.14 Diodeswere aimed at the limbus, and the amountof infrared light reflected from this regionwas monitored. The signals were propor¬tional to the angle of ocular rotation. Theresponse was linear over at least a ± 5°range of movements with a resolution of 10minutes of arc. An infrared emitter

mounted between the diodes diffusely illu¬minated the eye. The overall bandwidth ofthe recording system was 75 Hz (—3 dB). Achinrest and headrest, usually used with abite bar covered with dental impressionmaterial, stabilized the head.

A minicomputer was used to generate asmall (approximately 4 minutes), brighttest spot on a display screen placed either57 or 91 cm directly in front of the subjectalong the midline. Target luminance was

always maintained at least 1 log unit abovescreen luminance.

Fixational eye movements for the mid-line target position or 2.5° or 5.0° to eitherthe left or right of midline were testedduring monocular and binocular viewingconditions. During monocular testing, thenontested eye was prevented from seeingthe target by occlusion with either a blackeyepatch or a large partition. These meth¬ods of occlusion had no effect on eye move¬ments.

Subjects were obtained from either thegeneral refraction clinic or the orthopticsclinic at the School of Optometry. All hadthorough vision examinations and werefree of ocular or neurologic disease. Agesranged from 15 to 33 years, with a mean

age of 25.5 years. Subjects had either inter¬mittent strabismus, amblyopia withoutstrabismus, or constant strabismus am¬

blyopia. The prescribed spectacles orcontact lenses were worn during all test¬ing. Table 1 summarizes complete clinicaldata of the subjects. Each subject grantedinformed consent after the nature of theprocedure was fully explained.

RESULTS

The principal finding of our investi¬gation was the presence of saccadicintrusions during fixation in subjectswith strabismus. Saccadic intrusionswere found during most fixationconditions in three of four subjectswith intermittent strabismus. Theywere also prominent during monocu¬lar fixation with the amblyopic eye infour of five subjects with constantstrabismus with amblyopia. Saccadic

Accepted for publication Oct 19, 1978.From the School of Optometry, University of

California, Berkeley. Dr Ciuffreda is now withthe College of Optometry, State University ofNew York, New York. Dr Kenyon is now withMassachusetts Institute of Technology, Cam-bridge.

Reprint requests to College of Optometry,State University of New York, 100 E 24th St,New York, NY 10010 (Dr Ciuffreda).

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Table 1.—Clinical Data of Subjects*Subject/Age, yr Prescription

VisualAcuity

VergenceAbnormality

EccentricFixation

Correspon¬dence

Previous Surgery or

Orthoptics Therapy

1/25 OS +2.00 = -0.25X130OD +2.25

Constant Strabismus Amblyopia20/25 1-2AETOS & Nasal OS20/15

ARC Surgery, age 16

2/23 OS +3.75 = -0.50x165OD +0.50

20/3020/15

18 ET OS 1 Nasal OS Surgery, age 6

3/15 OS -1.50

OD -1.75

20/122

20/20

10 ET and1 HT OS

2.5 Nasal and2 superior OS

ARC No

4/32 OS +4.00OD plano

20/27720/20

4 ET OS 16 Nasal and4 superior OS

No

5/33 OS +0.75 = -0.50x40 20/630

OD +0.25 = -0.50x180 20/10

5-6 ET and2 HT OS

2.5-3.5 Nasaland 3-4 su¬

perior OS

Surgery, age 8

6/24 OS +-.75 = -2.00x90OP p1 =-0.50 X 19

Amblyopia Without Strabismus20/38 None 2 Nasal and20/20 2 inferior OS

NRC No

7/25 OS-2.50 = -1.25x172OD -5.00 = -0.75X5

20/2520/40

NoneNone

2 Nasal and2 inferior OD

NRC No

3/19 OS +5.00

OD +3.00

20/110

20/15

None 2 Temporal OS NRC Orthoptics therapy,age 17

Intermittent Strabismus With and Without Mild Amblyopia9/22 OS-0.75 = —0.25x148 20/20 18 ALT XT Slight unsteady

and 12 HT central OUOD-3.00 = -0.25X110 20/20

NRC No

10/31 OS-5.00OD-4.50 = -0.75x20

20/2020/20

15 XT OS Central, steadyOU

ARC Surgery, age 16

11/32 OS +0.75 = -1.75x180 20/20

OD +1.25 = -3.50X5 20/23

40-50 XT OD 1 Nasal andsuperior, OD

ARC Orthoptics therapy,age 32

12/25 OS piano

OD -1.00

20/32

20/16

10 XT and20 HT OS

Via Nasal, OS ARC No

•Abbreviations are as follows: ET, esotropia; HT, hypertropia; XT, exotropia; ALT, alternating; ARC, anomalous retinal correspondence; NRC, normalretinal correspondence; , prism diopter.

Fig 1 .—Eye position as function of time forsubject 9, who had intermittent strabismusand equal vision (20/20) in each eye. Fromtop to bottom, tracings are dominant lefteye during binocular fixation (slow chartspeed), dominant left eye during binocularfixation (fast chart speed), dominant lefteye during monocular fixation, and non-dominant right eye during monocular fixa¬tion. Saccadic intrusions are presentunder all viewing conditions and occur inthe absence of marked preceding drift ofeye. Symbols for this and subsequentfigures are T, templeward movement; N,nasalward movement; , eye position.Subscripts are o, fellow eye occluded; p,fellow eye patched; T, target; B, binocularfixation; N, monocular fixation with normal(dominant) eye; A, monocular fixation withamblyopic eye; ND, monocular fixationwith nondominant (20/20) eye; OD, righteye; and OS, left eye.

intrusions were rarely found in ourthree subjects with amblyopia withstrabismus. The initiation of saccadicintrusions did not depend on thepresence of considerable precedingdrift, ie, drift amplitudes comparablein magnitude to saccadic amplitudes.

In the vast majority of cases, theinitial saccade of the intrusion was notcorrective in nature.-

Intermittent StrabismusThree subjects with intermittent

strabismus exhibited saccadic intru-

sions under all test conditions. Forexample, subject 9, who had 20/20visual acuity in each eye, exhibitedsaccadic intrusions during monocularfixation with either eye as well as

during binocular fixation. This isclearly shown in Fig 1. In most

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Fig 2.—Monocular fixation amblyopic eye in subject 8, who had amblyopia without strabismus (20/110). Contrary to subjectswith strabismus, few saccadic intrusions are evident in subjects with amblyopia only, probably in no greater incidence thanfound in some normal subjects. Prominent features of record are increased drift amplitudes and velocities.

Fig 3.—Eye position as function of time forsubject 4, who had constant strabismusamblyopia (20/277). From top to bottom,tracings are left and right eye during bin¬ocular fixation, monocular fixation normaleye, and monocular fixation amblyopiceye. Note presence of saccadic intrusionsonly during monocular fixation with am¬blyopic eye.

Fig 4.—Monocular fixation amblyopic eye in subject 3, who had constant strabismusamblyopia (20/122). Trajectories and baselines of saccadic intrusions are clearly seenhere with faster chart speed.

instances, the intrusions occurredwithout the presence of markedpreceding drift. Although mean intru¬sion amplitude was greatest underbinocular fixation conditions, intru¬sion frequencies were similar (aboutone per second) for all test conditions.The fourth subject (No. 11), with mildamblyopia (20/32), had normal fixa¬tion under all test conditions.

Amblyopia Without Strabismus

Saccadic intrusions were rarelyfound in subjects having amblyopiawithout strabismus, probably in no

greater incidence than they might befound in normal subjects. A represen-

tative record is shown in Fig 2 forsubject 8. The prominent feature ofthe record is increased drift, with a

paucity of large fixational saccadespresent.

Constant Strabismus Amblyopia

Saccadic intrusions were found dur¬ing monocular fixation with theamblyopic eye in four of five subjects(No. 2 through No. 5) with constantstrabismus amblyopia. Only in subject2 were intrusions present during bin¬ocular fixation as well as duringmonocular fixation with the normal(dominant) eye. Eye movement rec¬ords for subject 4 (20/277) are

presented in Fig 3. The similarity ofthe left and right eye traces duringbinocular fixation to the trace formonocular fixation with the normaleye is evident. These three traces arein marked contrast to the fixationrecord for the amblyopic eye, where

templeward-initiated saccadic intru¬sions with amplitudes of Io to 2° are

present. Figure 4 shows the fixationrecord for subject 3 (20/122); more

typical nasalward-initiated saccadicintrusions with amplitudes of up to 4°occur at a rate of approximately one

per second. The 1° templeward shiftin baseline position that occurs mid¬way in the top trace suggests a smallchange in mean eccentric fixationlocus. A similar templeward fixationshift is also present in the lower trace(during seconds 2 and 3). There gener¬ally were steady intervals as long as 1s in duration between saccadic intru¬sions. Fixation was within normallimits under all test conditions insubject 1.

Group Data

The group data are presented in Fig5 and Table 2. In Fig 5, saccadicamplitude during fixation is plotted

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4.0

3.0 -

2.0 -

o

°

D

1.0

11

ID D

_L J_ I _L10 15 20 25 30

Visual Resolution, Minutes of Arc35 40

Fig 5.—Saccadic amplitude during fixationas function of visual resolution. Data arefrom Table 2. Open squares representmean saccadic amplitudes; filled squaresrepresent median saccadic amplitudes inamblyopic eyes for our subjects withconstant strabismus amblyopia. Trianglesrepresent mean amplitudes for temple-ward-directed saccades, and open circlesrepresent mean amplitudes for nasalward-directed saccades of Schor's" subjectswith constant strabismus amblyopia.Range of mean and median saccadicamplitudes for our intermittent strabismicsubjects for all test conditions is repre¬sented by vertical rectangle (in lower leftcorner). Saccadic amplitudes for oursubjects having amblyopia without strabis¬mus are represented by horizontal line(lower left corner); these are within normallimits. Note lack of direct relationshipbetween mean or median saccadic ampli¬tude and visual resolution in amblyopic (ornondominant) eye for our subjects. Cen¬tral tendencies are generally less than1°.

Table 2.—Saccadic Amplitude During Fixation in Patients With Strabismus*

Subject Mean ± 1 SD," Median,"Sample

Size FixationConstant Strabismus Amblyopia

<0.15WNL, A Midline0.6 ± 0.3 R, A 0.55 860.6 ± 0.2 L, A 0.55 780.4 ± 0.3 A 0.40 420.4 ± 0.2 A 0.40 300.4 ± 0.2 0.40 200.3 ± 0.2 0.25 12

MidlineMidlineMidline5° Left2.5° LeftMidline

1.5 ± 0.7 A 1.75 84 Midline0.7 ± 0.4 L, A 0.65 420.5 ± 0.3 R, A 0.35 220.5 ± 0.3 A 0.30 73

MidlineMidlineMidline

0.8 ± 0.8 A 0.70 320.8 ± 0.7 A 0.700.5 ± 0.3 A 0.35 42

MidlineMidlineMidline

6-8Amblyopia Without Strabismus

<0.15WNL, A MidlineIntermittent Strabismus With and Without Mild

0.6 ± 0.2 "A" 0.60Amblyopia

150.5 ± 0.2 0.45 170.9 ± 0.6 0.85

MidlineMidlineMidline

10 0.6 ± 0.3 "A" 0.50 540.4 ± 0.2 0.35 270.4 ± 0.2 0.40 39

MidlineMidlineMidline

<0.15 WNL, A<0.15 WNL,

MidlineMidline

12 0.3 ± 0.1 A 0.30 360.4 ± 0.1 0.35

MidlineMidline

"A indicates amblyopic eye; N, normal or dominant eye; B, binocular viewing; WNL, within normallimits; "A," nondominant eye of intermittent strabismic; R, saccades directed to the right; and L,saccades directed to the left.

as a function of visual resolution. Forsubjects with both intermittent andconstant strabismus, the central ten¬dencies were typically 1° or less inamplitude. Thus, there was no directrelationship between saccadic ampli-

tude during fixation and visual resolu¬tion. Subjects having amblyopia with¬out strabismus exhibited fixationalsaccades that were within normalamplitude limits (generally less than20 minutes).

Extensive Observations ofFixation in a High Amblyope

Fixational eye movements in sub¬ject 5, who had constant strabismusamblyopia (20/630), were studied un¬der a variety of test conditions.Figure 6 (upper trace) shows monocu¬lar fixation with the amblyopic eye inwhich saccadic intrusions, single sac-

cades, and drifts are present. Portionsof this trace provide a good exampleof the steady fixation that was attimes found in this high amblyope. Atother times, saccadic intrusions were

frequently observed. Saccadic intru¬sions could be elicited by redirectingthe subject's attention to the fixationtask, as shown in Fig 6 (lower trace).At the arrow, the experimenter ver¬

bally reminded the subject to continuelooking closely at the target; a briefperiod of intrusions ensued. Interest¬ingly, changes in instruction to stra¬bismic or amblyopic subjects from"fixate carefully on the target" to"hold the eye steady" (in the presenceof the target) could decrease fixation¬al saccadic frequency by 50% to 90%,similar to that found for normalpersons15; this has been reported else¬where.116 Large refixation saccadeswere also present following stepchanges in target position (Fig 7).After steady fixation for severalseconds, a 5° step change in targetposition was introduced. This resultedin a series of saccades rather than a

single saccade to refixate the target.Fixation ability was tested in stillanother way. The display screen andsurrounding laboratory equipmentcould be seen by the subject in the

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Fig 6.—Monocular fixation amblyopic eyein subject 5, with constant strabismusamblyopia (20/630). Upper trace showsremarkable steadiness (seen at times) ofeye considering visual acuity is so low. Inlower trace (at arrow), steadiness of fixa¬tion was disrupted when experimenterspoke to subject and redirected subject'sattention to task. Baseline fixation area

following these intrusions was approxi¬mately 1.5° more nasal.

Fig 7.—Monocular fixation amblyopic eyein subject 5, with constant strabismusamblyopia (20/630). Note relative steadi¬ness of eye before and shortly after 5°change in stimulus position was intro¬duced; in contrast, several refixationsaccades occurred for a few seconds aftertarget jump. Large deflections that movedpen off chart were due to blinks. L, left.

darkened room. The subject was askedto fixate the midline target. Afterseveral seconds the target was extin¬guished, and the subject was in¬structed to fixate where the targethas previously appeared. The result¬ing amblyopic eye fixation pattern isshown in Fig 8. It is clear that thesubject could not in this situationmaintain as stable an eye position aswhen the fixation target was present;the presence of a target (visual feed¬back) appeared to aid in maintenanceof steady fixation. Finally, the subjectsometimes noted that the targetappeared to "fade out" and disappearfor short periods. To determinewhether eye movements were relatedto target disappearance, we in¬structed the subject to look intently atthe target and depress a switch held inthe right hand whenever the targetwas no longer visible (the "Lawwill

experiment"17)- The results are pre¬sented in Fig 9. We initiated measure¬ment by allowing for an assumed eye-hand two-choice reaction time of 350ms." On the average, approximately100 ms following target disappearancethe amblyopic eye began to driftnasally with an average velocity of1.0° per second; it continued to do sowith an average amplitude of 2.5°until the target was once again visi¬ble. The accumulated eye positionerror was corrected by either a singlelarge saccade or, more typically, bymultiple refixation saccades similar tothose seen in Fig 6 and 7 where thesubject's attention was redirected.

COMMENTThe preceding data illustrate rather

clearly that the presence of saccadicintrusions was related to strabismusand not amblyopia. These findings

confirm those of others regarding thepresence of saccadic intrusions inconstant strabismic amblyopia; butmore importantly, they extend it toinclude subjects with intermittentstrabismus and exclude those withamblyopia alone. Thus, for presum¬ably the first time, a relationshipbetween saccadic intrusions and stra¬bismus is clearly demonstrated.

Visual Acuity Unaffected bySaccadic Intrusions

That intrusions do not adverselyaffect visual acuity was supported bythe finding that they occurred insubjects with intermittent strabismushaving normal visual acuity in eacheye (20/20). Furthermore, we haverecorded saccadic intrusions duringfixation in subjects with normal visualacuity free from strabismus, amblyo¬pia, or neurologic disease (unpublished

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Fig 8—Monocular fixation amblyopic eye in subject 5, with constant strabismus amblyopia (20/630).Subject was instructed to fixate where small target appeared before it was extinguished. Largesaccadic intrusions, drift, and baseline changes indicate subject could not perform task well.

Fig 9—Monocular fixation amblyopic eye in subject 5, with constant strabismus amblyopia (20/630)during objective demonstration of the Lawwill experiment. Lower trace is eye position, and upper trace isevent marker indicating when target is not visible to subject. Note drift of eye after target disappears andsaccadic return of eye toward center of screen when target is again visible.

data). This lack of interference bysaccadic intrusions on visual acuityappears reasonable, since the intersac-cadic interval for an intrusion was

rarely shorter than 100 ms or longerthan 400 ms, thereby allowing ade¬quate visual processing time duringthese periods. Furthermore, since in¬trusions generally averaged less than1° in amplitude, the change in visualresolution for those retinal areas usedduring the intrusion relative to thepreferred fixation locus would notseriously impair resolving ability. Infact, it appeared to go unnoticed inour strabismic subjects during ev¬

eryday binocular viewing conditions.Moreover, since saccadic intrusionfrequency ranged from 0.3 to 2.0 persecond, the interval during which a

target and preferred fixation locuswould be coincident also provided an

adequate processing period. This lackof affect of saccadic intrusions onvisual acuity in strabismics agreeswith recent findings by Hess,'2 who, ina tangentially related study, foundsimilar contrast thresholds in am¬

blyopic eyes during both stabilizedand normal viewing conditions. Thefact that intrusion direction in theamblyopic eye frequently (more than70% of the time) occurred in the samedirection as the squint suggests afixation bias induced by the strabis¬mus. Subjects with constant exotropiamust be carefully studied and consist-

ent results obtained before this hy¬pothesis can gain support.

No Relationship Between SaccadicIntrusion Amplitude and VisualAcuity and No Support for the

Asymmetric 'Dead Zone' TheoryCan the amplitude of saccadic

movements during fixation in an

amblyopic eye be predicted based onlyon its visual resolution? We found no

relationship between mean or mediansaccadic amplitude and visual resolu¬tion in the amblyopic eye for eithergroup of subjects with strabismus(Fig 5). This result is in strikingcontrast to the findings of Schor andFlom," who found a high correlationbetween these two variables in fiveconstant strabismic amblyopes inwhom median saccadic amplitude in¬creased as visual acuity in theamblyopic eye decreased. They alsodeveloped a mathematic expression topredict median saccadic amplitudeduring fixation in the amblyopic eyebased simply on visual resolution. Thelack of agreement between the data ofour subjects with constant strabismusand high amblyopia and theirs demon¬strates the necessity of testing a largegroup of subjects before attemptingto develop a general mathematicexpression with high predictive powerto relate eye movements to visualacuity in amblyopes.

Saccadic intrusions appear to be

unrelated to abnormal eye positionerror detection in the amblyopic eyeresulting from an asymmetric deadzone (believed to be due to hemiretinalsuppression in the deviated eye).1 ' Nordoes it appear to be related to functionto correct for drift-induced positionerrors. This lack of correlation issuggested by several lines of informa¬tion: (1) Subjects were able to followrandom target step displacements tothe left or right as small as 0.4° inamplitude. (2) In many instances, thebaseline position before and immedi¬ately after completion of a saccadicintrusion was similar, even thoughsaccadic intrusion amplitudes showedmuch variability. (If a true dead zone

existed, mean intrusion amplitudeswould exhibit little variability.) (3) Inmany instances, considerable drift didnot precede initiation of the intrusion.(4) When drifts did occur, the accumu¬lated position error was usually cor¬rected by a single, large saccade.(These could be as small as 5 minutesin amplitude, as measured duringhigh-gain recordings.) Schor andFlom1' hypothesized that error-pro¬ducing saccades were initiated toplace the retinal image of the targetoutside this asymmetric dead zone,thus allowing the amblyopic eye todetect and correct the position error.On our reexamination of the origi¬nal data,19 we detected the presence offrequent large saccadic intrusions in

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the nonamblyopic eye during monocu¬lar fixation in some of their subjects.This does not support the dead zone

hypothesis for the generation ofsaccadic intrusions, but it agrees withour finding of saccadic intrusionsduring monocular and binocular fixa¬tion in subjects with strabismus, espe¬cially of the intermittent variety.

The Lawwill 'Fading' ExperimentLawwill17 made some interesting

observations on amblyopic subjectsthat may provide a clue regarding a

possible function of saccadic intru¬sions. While his subjects viewedletters on a distance acuity chartthrough a half-silvered mirror withthe amblyopic eye, he viewed thefundus (of the amblyopic eye) with aninfrared ophthalmoscope. He notedperiods of steadiness along with inter¬vals when the eye was estimated tohave drifted as much as 2° beforesubsequent movements returned theeye to the target. At times, thesubjects reported fading of the target.Lawwill noted that the report offading occurred as ocular drift began.The target reappeared at the end ofthe drift. He hypothesized that fadingof the image may be due to an acceler¬ated regional visual adaptation inamblyopic eyes and conducted otherexperiments that supported this hy¬pothesis. While performing a similar

experiment on one of our subjects, weconfirmed Lawwill's experimental eyemovement observations and, more

importantly, succeeded in quantifyingthis phenomenon. Fading of the fixa¬tion target appears to initiate theocular drift. Reappearance of thetarget, once it extends beyond thisregion of rapid adaptation, initiatesthe saccadic return movements. Thus,Lawwill's hypothesis appears to be themost likely explanation for theseresults.

How does this information relate togeneration of saccadic intrusions? Onefunction served by fixational eyemovements in normal persons (usuallyoccurring within an area less than 10minutes in angular extent'-'") is toprevent visual adaptation. Artificialretinal image stabilization results inrapid disappearance of a target.21Execution of frequent saccadic intru¬sions may be one way to preventfading of the retinal image due toabnormally rapid visual adaptationoccurring over small regions of theeye. Therefore, as has been suggestedelsewhere,1 '- this may be an adaptivephenomenon. These local regionsprobably coincide with retinal areasthat undergo suppression under binoc¬ular conditions in the deviated eye.The occurrence of intrusions in someof these subjects during fixation withthe dominant eye or during binocular

viewing, even though infrequent, sug¬gests that the presence of strabismusmay adversely affect oculomotor con¬trol during fixation in each eye, andthus may enter as a second factor inthe generation of saccadic intrusions.

Saccadic Intrusions inIntermittent Strabismus

As was hypothesized in constantstrabismus amblyopia, saccadic intru¬sions could result from abnormallyrapid regional visual adaptation. Atthose times when the visual axes are

divergent, ie, in exotropia, regions ofthe deviating eye typically undergosuppression.2224 The suppression thatoccurs in these subjects, while produc¬ing little, if any, amblyopia in eithereye because of the intermittentnature of the defect, may still producesubtle abnormalities as early as theretinal level with a possible conse¬

quence being abnormally rapid re¬

gional visual adaptation. Moving theeyes over small angular extents helpsprevent the image from fading. And,as hypothesized for a minority ofsubjects with constant strabismusamblyopia, the presence of strabismusmay simply degrade fixation ability inboth eyes.

This investigation was supported in part bytraining grant Ey-00076 from the National EyeInstitute.

References

1. Ciuffreda KJ: Eye Movements in Amblyopiaand Strabismus, thesis. School of Optometry,University of California, Berkeley, 1977.

2. Daroff RB: Ocular oscillations. Ann OtolRhinol Laryngol 86:102-107, 1977.

3. Atkin A, Bender MB: "Lightening eyemovements" (ocular myoclonus). J Neurol Sci1:2-12, 1964.

4. Baloh RW, Konrad HR, Honrubia V: Vestib-ulo-ocular function in patients with cerebellaratrophy. Neurology 25:160-168, 1975.

5. Alpert JN, Coats AC, Perusquia E: "Saccad-ic nystagmus" in cerebellar atrophy. Neurology25:676-680, 1975.

6. Selhorst JB, Stark L, Ochs AL, et al: Disor-ders in cerebellar ocular motor control: II. Macro-saccadic oscillation an oculographic control sys-tem and clinico-anatomical analysis. Brain99:509-522, 1976.

7. Jung R, Kornhuber HH: Results of electro-nystagmography in man: The value of optokinet-ic, vestibular, and spontaneous nystagmus forneurologic diagnosis and research, in Bender M(ed): The Oculomotor System. New York, Harper& Row Publishers, 1964.

8. Feldon SE, Langston JW: Square-wavejerks: A disorder of microsaccades? Neurology

27:278-281, 1977.9. Mackensen G: Das fixationsverhalten am-

blyopischer Augen. Albrecht von Graefes ArchOphthalmol 159:200-211, 1957.

10. von Noorden G, Mackensen G: Phenome-nology of eccentric fixation. Am J Ophthalmol53:642-661, 1962.

11. Von Noorden G, Burian HM: An electro-oculographic study of the behavior of the fixationof amblyopic eyes in light- and dark-adaptedstate: A preliminary report. Am J Ophthalmol46:68-77, 1958.

12. Hess RF: Eye movements and gratingacuity in strabismic amblyopia. Ophthalmic Res9:225-237, 1977.

13. Schor C, Flom MC: Eye position control andvisual acuity in strabismus amblyopia, in Lenner-strand G, Bach-y-rita P (eds): Basic Mechanismsof Ocular Motility and Their Clinical Implica-tions. New York, Peragmon Press, 1975.

14. Stark L, Vossius G, Young LR: Predictivecontrol of eye tracking movements. Inst RadioEng Trans Hum Factors Electron 3:52-57, 1962.

15. Steinman RM, Cunitz RJ, Timberlake GT,et al: Voluntary control of microsaccades duringmaintained monocular fixation. Science 155:1577\x=req-\1579, 1967.

16. Ciuffreda KJ, Kenyon RV, Stark L:Suppression of saccadic intrusions in strabismicand anisometropic amblyopia. Ophthalmic Res11:31-39, 1979.

17. Lawwill T: Local adaptation in functionalamblyopia. Am J Ophthalmol 65:903-906, 1968.

18. McCormick EJ: Human Factors in Engi-neering and Design, ed 4. New York, McGraw\x=req-\Hill Book Co, 1976, p 185.

19. Schor C: Oculomotor and NeurosensoryAnalysis ofAmblyopia, thesis. School of Optome-try, University of California, Berkeley, 1972.

20. Ratliff F, Riggs LA: Involuntary motion ofthe eye during monocular fixation. J Exp Psychol40:687-701, 1950.

21. Ditchburn RW: Eye Movements and VisualPerception. Oxford, England, Clarendon Press,1973.

22. Jampolsky A: Characteristics of suppres-sion in strabismus. Arch Ophthalmol 54:683-696,1955.

23. Nawratzki I, Jampolsky A: Regional hemi-retinal difference in amblyopia. Am J Ophthal-mol 46:339-344, 1958.

24. Pratt-Johnson J, Wee HS: Suppressionassociated with exotropia. Can J Ophthalmol4:136-144, 1969.

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