Dynamic Vergence Eye Movements in Strabismus and Amblyopia: Symmetric Vergence

Dynamic vergence eye movements in strabismus and amblyopia: symmetric vergence

Robert V. Kenyan, Kenneth J. Ciujfreda,* and Lawrence Stark

Dynamic vergence eye movements in response to step target displacements along the midline were measured by an infrared reflection technique in 11 patients having either intermittent strabismus, constant-strabismus amblyopia, or amblyopia without strabismus. We found the absence of normal disparity (fusional) vergence in all patients having strabismus and in some patients having amblyopia without strabismus. A characteristic response consisting of a binocular accommodative vergence component and an early binocular saccadic component was used to foveate the target of interest with the dominant eye. Vergence responses in our control subjects and patients with the nondominant eye occluded were similar to those recorded in our patients during binocular vieioing. These results suggest that disparity information is not utilized by patients, probably as a result of long-term, ongoing suppression in the deviated or amblyopic eye. Accommodative vergence with the aid of an early foveating saccade was the primary mechanism for tracking targets in three-dimensional space.

Key words: strabismus, amblyopia, vergence, eye movements, Hering's law, accommodation

V,ergence eye movements in patients with lieved that some strabismic patients could strabismus and amblyopia have been inferred produce "fusional movements" when dispa- from patients' subjective responses to disparate stimuli, placed in the peripheral retina of rate stimuli presented simultaneously to each each eye, were reported fused. Patients re- eye, rather than objectively recorded and ported changes in the localization of two hap- quantified (for a review of early work, see lopic fiduciary marks located in the center of Burian and von Noorden1). Burian,2 follow- the visual field, and this was interpreted as ing Bielschowsky3 and Schlodtmann,4 be- evidence for actual eye rotations. Hallden5 confirmed Burian's finding in patients having anomalous retinal correspondence (ARC). He From the School of Optometry, University of California, similarly defined fusional movements as a re- Berkeley. turn to the no-disparity condition in the cen- This research was supported by N.I.H. training grant tral field following the introduction of a dis- EY00076 (R. V. K. and K. J. C.) and an Auxiliary to parity. In Hallden's study, changes in sub- the American Optometric Association Research grant jective localization of targets were estimated (K. J. C). Submitted for publication July 26, 1978. by haploscopic techniques, and from this he Reprint requests: Robert V. Kenyon, Man-Vehicle Lab- calculated changes in vergence angle. These oratory, Department of Aeronautics and Astronautics, fusional movements took several minutes to Room 37-215, Massachusetts Institute of Technology, complete, and static measurements of target Cambridge, Mass. 02139. locations were made only about once a min- *Present address: Department of Basic Optometric Sci- ute. However, in none of the above studies ences, State College of Optometry, State University of New York, 100 E. 24th St., New York, N. Y. 10010. were eye movements objectively recorded.

Mariani and Pasino6 criticized Burian's eye would only be 0.01 mm or 0.05° for a 10° study and pointed out that other factors could rotation, below the noise level of our recording account for his results. They referred to system. Kretschemer,7 who showed that changes in To ensure that the responses were independent the angle of anomaly rather than true fusional of the target system, two systems were used to movements could be the mechanism em- stimulate vergence. In each system, targets were placed along the subject's midline at 25 and 50 cm ployed to fuse disparate targets. (The angle of away from the estimated center of rotation of each anomaly is measured from the fovea in the eye. These targets were carefully adjusted in both nondominant eye to a point in the nondomi- horizontal and vertical planes to minimize occur- nant eye that corresponds to the same visual rence of eye movements resulting from target direction as the fovea of the dominant eye.) misalignment. In one system, the two targets From their own experiments on fusion in consisted of small Lucite plates with fine crosses strabismic patients, still without objective etched in the front surfaces subtending visual an- eye movement recordings, Mariani and Pa- gles of 1.5° and 3.0° for the far and near targets, sino6 inferred that most patients changed the respectively. The fine lines of the crosses sub- angle of anomaly instead of performing true tended angles of 2 and 4 min arc for the near and far targets, respectively. A miniature bulb (GE fusional movements, thus confirming Kret- 222) was installed to provide target illumination of schemer's findings. the etched cross alone. In the other system, In an attempt to reconcile these differ- targets were made from strips of exposed film with ences and further extend these observations, fine crosses etched into the emulsion, and the we objectively recorded dynamic vergence targets were mounted in front of a 2 cm square eye movements in 11 patients having ei- holder and back-illuminated by a grain-of-wheat ther constant-strabismus amblyopia, ambly- filament bulb through a light diffuser. The holders opia without strabismus, or intermittent for the far and near targets subtended angles of strabismus, while changing binocular fixation 2.3° and 4.5°, respectively. The fine lines compos- ing the crosses subtended angles of 2 and 4 min arc between near and far midline targets. These for far and near targets, respectively. targets produced disparity by changing dis- The luminance of the targets was measured tance from the patients as is found in normal with an S.E.I, photometer under the same low everyday binocular viewing. Quantification photopic illumination conditions used during the of the dynamic aspects of the vergence re- experiments. The luminance for the Lucite plates sponse in these patients shows the absence of measured 0.5 log ft-lamberts. The contrast for normal disparity vergence movements and these targets with the formula (lmax — tarn/Lax + the use of normal accommodative vergence Imin) was 0.53. For the second system using the eye movements and saccades to track targets exposed film, the target luminance measured 1.7 in three-dimensional space. log ft-lamberts and the contrast was 0.93. Experimental procedures were adapted to the clinical situation and thus kept as simple and as Methods uniform as possible. Targets were alternately il- Binocular horizontal eye position was recorded luminated in a pseudorandom sequence by the by an infrared reflection method.8- 9 The recording experimenter. Each subject was instructed to system had an overall bandwidth of 150 Hz, a lin- keep the illuminated target clear and single at all ear range of at least ±7°, and a noise level of 6 min times. These procedures were performed (1) with arc. The infrared method does not distinguish be- both eyes viewing and (2) with the nondominant tween eye rotation and eye translation; hence, eye covered but still allowing eye movements to translational movements, if large enough, could be recorded from both eyes. Calibrations were introduce artifacts in the eye movement record- performed before, during, and after each brief ex- ings. However, Krishnan and Stark,10 using a perimental run. method that distinguishes between rotation and Eleven patients having strabismus and/or func- translation, have shown that eye translation during tional amblyopia and two normal control subjects saccadic or vergence eye movements is minimal. participated in the study. Patients were recruited Furthermore, using data from Fry and Hill," they from the general clinic at the School of Op- estimated that the translational movement of the tometry, University of California, Berkeley. All Invest. Ophthalmol. Vis. Sci. 62 Kenyon, Ciuffreda, and Stark January 1980

Table I. Clinical data of subjects

Visual Vergence Eccentric Correspondence Subject Age Prescription acuity abnormality fixation and stereoacuity* Constant-strabismus amblyopia: B. S. 25 LE +2.00 = -0.25 x 130 20/25 1-2* ET LE V2* nasal LE ARC RE +2.25 20/15 200" D. F. 23 LE +3.75 = -0.50 x 165 20/30 18* ET LE 1* nasal LE RE +0.50 20/15 400" J. K. 15 LE -1.50 20/122 10* ET LE; 2.5* nasal; ARC RE -1.75 20/20 1* HT LE 2* superior LE 300" B. B. 33 LE +0.75 = -0.50 x 40 20/630 5-6*ETLE; 2.5^.5* nasal; — RE +0.25 = -0.50 x 180 20/10 2* HT LE 3-4* superior LE — Amblyopia without strabismus: S. H. 24 LE -0.75 = -2.00 x 90 20/38 None 2* nasal; 2* NRC RE pi = -0.50 x 19 20/20 inferior LE 100" L. T. 25 LE -2.50 = -1.25 x 172 20/25 None 2* Nasal; 2* NRC RE -5.00 = -0.75 x 5 20/40 inferior RE 60" B. W. 19 LE +5.00 20/110 None 2* temporal LE NRC RE +3.00 20/15 400" -> 60" Intermittent strabismus without amblyopia: J. L. 13 LE +0.75 20/20 20* ET RE; Jerk nyst. UHARCt RE +0.50 20/20 6* HT RE — B. N. 31 LE -5.00 20/20 15* XT LE Central, steady ARC RE -4.50 - -0.75 x 20 20/20 LE, RE 40" Former strabismus patients: J. W. 24 LE -5.00 20/15 6*EPH None NRC RE -2.50 = 0.75 x 165 20/25 140" J. B. 25 LE -0.75 = -0.50 x 8 20/25 10* EXPH None NRC RE -2.75 = -0.75 x 90 20/30 2*HPH — Control subjects: B. L. 29 LE Piano 20/20 None None NRC RE Piano 20/20 40" A. D. 23 LE +8.0 == 0.25 x 175 20/20 None None NRC RE +8.0 20/20 40"

ET = esotropia; XT = exotropia; ARC = anomalous retinal correspondence; NRC = normal retinal correspondence. *At least as indicated. tUnharmonious ARC. patients had a thorough vision examination and It should be noted that what is called "dispar- were free from ocular or neurological disease. ity" vergence in this paper has been known as They were classified into three major groups: "fusional" vergence in the past. We prefer to use constant strabismus with varying degrees of am- the term disparity rather than fusional because blyopia, amblyopia without strabismus, and in- disparity drives the vergence system and fusion is termittent strabismus without amblyopia. In some usually a higher-level perceptual result following patients classified as amblyopic, the visual acuities these movements. were less than 20/40 in the nondominant eye. In these cases, the criterion of a two-line difference Results between the visual acuities of the two eyes was used to define amblyopia. This method is standard Absence of disparity vergence in patients. clinical practice.12' l3 The subjects' ages ranged Typical disparity vergence eye movements from 10 to 33 years, with an average age of 25. A produced by changing fixation between near summary of each subject's clinical findings is pre- and far midline targets were characterized by sented in Table I. a 160 to 200 msec latency followed by Volume 19 Number 1 Symmetric vergence in strabismus, amblyopia 63

amplitude of the dominant eye was approxi- Vergence abilities mately 18% of that of the fellow eye. In these responses, the unequal vergences were ac- 40 cm 6 m companied by a binocular saccade that served Base tnA Base in Previous Base out* Base out* to place the fovea of the dominant eye close surgery or (break/ (break/ to the new target. The combination of this therapy refusion) refusion) saccade and the small amplitude vergence functioned to place and maintain the domi- Age 16 nant eye on the new target. Surgery 8/4 14/8 This pattern of unequal vergence am- Age 6 18/10 — Surgery 6/2 — plitudes accompanied by a saccade charac- None 24/14 15/10 terized all the responses made by patients 24/15 6/3 Age 8 — — having intermittent strabismus without am- Surgery — — blyopia. Eye movement responses in Fig. 1, b, display the typical response found in None 24/16 36/26 Patient B. N. (see Table I) and the other pa- 14/10 4/2 tient in this diagnostic group. In each re- None 38/10 32/14 27/22 4/2 sponse, the vergence in the dominant eye Age 17 — — was much less than that found in the fellow Orthoptics — — eye. For example, the convergence amplitudes in Fig. 1, b equaled 0.8° and 9.0° for Age 2 Surgery — — the dominant and nondominant eyes, re- Age 16 40/doubled 40/doubled spectively. For both convergence and di- Surgery 24/doubled 8/doubled vergence responses, the percent vergence amplitude in the dominant eye equaled 11% Age 3 28/18 16/10 of that found in the nondominant eye. Surgery 32/18 32/30 Age 8 — — Patients with constant-strabismus ambly- Surgery — — opia responded similarly. A representative example is seen in the eye movement re- None sponses of Subject J. K. (Fig. 2, a). Re- None sponses showed an absence of normal disparity vergence similar to those found in the previous patient (Fig. 1, b), having intermittent strabismus. Here, too, the unequal vergence amplitudes that occurred during both convergence and divergence, had lower am- smooth, equal, disjunctive movement of the plitudes in the dominant left eye than in the eyes.14"18 The response in Fig. 1, a, of a con- fellow eye. For example, the convergence trol subject exemplifies a normal response. amplitudes equaled 0.8° and 4.5° for the At times, the vergence contained a small sac- dominant and nondominant eyes, respec- cade as seen during the divergence response tively. For these records, dominant eye ver- of Fig. 1, a. gence amplitudes measured 18% of those in In contrast, most patients with strabismus the fellow eye for both the convergence and and/or amblyopia did not perform normal divergence. disparity vergence responses. Although the In contrast to patients with strabismus, not latencies were normal, these patients made all amblyopic patients exhibited these ab- unequal vergence movements in each eye as normal vergence repsponses. Of three pa- shown in Fig. 1, b. The vergence amplitudes tients having amblyopia without strabismus, were always smaller in the dominant eye than only L. T. performed normal vergence re- in the fellow eye; the average vergence sponses at all times; another amblyope, Invest. Ophthalmol. Vis. Sci. 64 Kenyon, Ciuffreda, and Stark January 1980

°RE * °T NEAR

500 ms -f+14+*++1 LF

'RE l *-_.-

'< i_ •"V I F1J • r - 4 ; 500 m«

Fig. 1. Symmetric vergence condition. Symbols for all figures unless otherwise noted: 0Le = left eye position; BRe = right eye position; 0^ = left eye velocity; 0Re + 0T = right eye velocity summed with target position. Downward deflections represent rightward movements; calibration bars for position represent 2°, and time markers represent 500 msec, a, Control Subject B. L. shows normal response to symmetric vergence stimuli, b, Patient B. N. having intermittent strabismus without amblyopia exhibits abnormal response, contrary to normal control subject responses in a. Following target changes, vergence occurs primarily in left eye only. Saccade occurring early in response is used to foveate new target with right eye; note unequal saccades occurring during vergence response, but equal saccades during extended fixation periods.

B. W., always produced abnormal vergence gence stimuli resembled those responses responses similar to those of the strabismic produced by all strabismic patients and some patients; the last amblyope, S. H., had brief nonstrabismic amblyopic patients under bin- intermittent episodes of normal vergence but ocular viewing conditions. The response of only during convergence. Eye movements Control Subject B. L. with the right eye cov- from Patient S. H. are shown in Fig. 2, h; the ered is shown in Fig. 3. The vergence re- vergence amplitudes in the dominant eye sponses seen in this figure contained only an equaled 6% of those in the amblyopic eye. accommodative vergence component due to Monocular viewing of midline targets. the occlusion of one eye. This is to be ex- When one eye was occluded, the responses pected since disparity vergence requires a of the control subjects to the symmetric ver- binocular stimulus; occluding one eye dis- Volume 19 Number 1 Symmetric vergence in strabismus, amblyopia 65

©LE

ORE

NEAR ©RE • eT FAR

500 mi

Fig. 2. Symmetric vergence condition, a, Patient J. K. with constant strabismus amblyopia, showing similar abnormal responses consisting of predominant vergence in amblyopic left eye, early foveating saccade in dominant right eye, and non-Hering's law saccades during response, especially for convergence, b, Patient S. H. having amblyopia without strabismus. Similar abnormal responses also found in this patient, but they only occurred intermittently. ables the disparity vergence control system. {Figs. 1, b, and 2). Each contained unequal Characteristically, the amplitude is smaller in vergence; the smaller amplitude occurred in the viewing eye than in the covered eye dur- the viewing eye for the control subject and in ing accommodative vergence.9j 19 For in- the dominant eye for the patients; and finally, stance, the amplitude of the accommodative each used a saccade to bring the fovea of the vergence movements in Fig. 3 equaled 4.2° dominant eye near the new target. in the covered eye and 1.2° in the view- When patients with strabismus and/or ing eye for both convergence and diver- amblyopia were monocularly occluded, so gence. The binocular saccade, due to the ret- that only the dominant eye viewed the inal error in the viewing eye, moves the fovea symmetrically positioned targets, responses of the dominant eye close to the new target. agreed both qualitatively and quantitatively Both qualitatively and quantitatively, the re- with the symmetric vergence responses from sponses from the control subjects' monocular these patients under binocular viewing con- tracking were similar to those recorded in our ditions. As with the control subjects, block- patients under binocular viewing conditions ing of one eye caused accommodation to Invest. Ophtfialmol. Vis. Sci. 66 Kenyon, Ciuffreda, and Stark January 1980

500 m»

Fig. 3. Monocular tracking of midline targets with dominant eye. Normal Control Subject B. L. with left eye occluded. Note vergence occurring predominantly in occluded eye; viewing eye saccade is used to foveate new target. drive vergence, producing unequal vergence under these conditions appeared similar amplitudes. The monocular retinal error to the accommodative vergence responses produced by the target change caused a bin- found in normals. Typical accommodative ocular saccade placing the dominant eye on vergence responses from our patients are the new target. shown in Fig. 4, b. This figure shows the eye Monocular line of sight targets. To study movement response of Patient B. N. exhibit- the ability of these patients to make normal ing normal characteristics of accommodative accommodative vergence responses, the tar- vergence: smaller amplitude vergence in the gets were carefully aligned along the visual viewing eye (25% of the amplitude in the axis of the dominant eye with the fellow eye covered eye) and corrective eye movement occluded, (the Miiller experiment).19 Under patterns.9 In general, accommodative ver- this condition, a large accommodative vergence with the dominant eye viewing was gence response occurs in the covered non- normal in all patients. dominant eye.19 We have recently shown Special cases. Neither degree of strabis- that besides the large vergence in the cov- mus nor grade of amblyopia in patients with ered eye, the viewing eye makes small ver- constant strabismus amblyopia had any effect gence responses approximately 12% of the on the responses to the symmetric vergence amplitude of that measured in the covered stimuli. Patients with small-angle strabismus eye.9 A clear example of this accommodative and deep amblyopia (B. B.) produced sym- vergence movement is seen in the responses metric vergence responses similar to those of from Control Subject B. L. (Fig. 4, a). In the patients who had mild amblyopia and small- divergence response, the small vergence in angle strabismus (B. S.). Furthermore, the the viewing eye equaled 25% of that found in presence of ARC, as found for Patient B. S. the covered eye. The small corrective sac- but not B. B., did not alter the basic re- cades were used to keep the viewing eye on sponse. the target and thus counteracted the small Within our group of patients, three were vergence driving the viewing eye away from successfully treated for amblyopia or strabis- the target. The responses from our patients mus. Patient B. W. received orthoptics ther- Volume 19 Number 1 Symmetric vergence in strabismus, amblyopia 67

'LE

3RE

FAR °RE * °T NEAR fj

500 ms

FLE

LE I

tf 500 ms

Fig. 4. Accommodative vergence with dominant eye viewing, a, Normal Control Subject B. L., with left eye occluded. Note vergence occurring primarily in occluded eye and small vergence in viewing eye, similar to that recently reported in other normal subjects.9 b, Patient B. N. having intermittent strabismus without amblyopia. Accommodative vergence shows normal dynamical response characteristics. apy for amblyopia and eccentric fixation in responses. Patient J. B, who now has an the left eye. After training, his visual acuity exophoria was operated on at age 8 to correct increased from 20/110 to 20/20, and his ec- a squint of his left eye. His symmetric ver- centric fixation reduced from 2 prism diop- gence responses were similar to those of the ters (PD) to zero. His vergence movements, other patients in our study having strabismus recorded shortly after termination of orthop- but who were not surgically corrected. How- tics treatment, contained the same character- ever, another patient, J. W., who had an eso- istic abnormal vergence response recorded in tropia surgically corrected at age 3 and pres- most of our patients. Thus, even after nor- ently has an esophoria, had intermittent malization of visual acuity and centralization episodes of normal convergence interspersed of fixation, normal disparity vergence re- with more frequent abnormal responses. sponses were never recorded in this former Non—Hering's law saccades during ver- amblyope. Interestingly, some other oculo- gence. During the analysis of vergence re- motor findings such as saccadic latency responses from both patients and control sub- mained abnormal in this patient during jects, we found that saccades which occurred and subsequent to successful amblyopia during vergence were often unequal in each 20 22 therapy. " eye. Fig. 5 shows symmetric vergence re- Patients with a history of strabismus as a sponses that contained saccades during dis- child and surgical correction to reduce the parity vergence from the control subjects. Al- strabismus were also included in our sample though the vergences in each eye were and showed the typical abnormal vergence approximately equal, the saccades were Invest. Ophthalmol. Vis. Sci. 68 Kenyon, Ciuffreda, and Stark January 1980

right eye, whereas it appeared in the left eye for the previous pair. This same pattern was repeated in the divergence response. The saccadic properties found during vergence in all subjects were best illustrated by the responses of control subject B. L. (Fig. 5, b). The divergence response showed dramatic differences in the amplitudes of the first sac- *« cadic pair during vergence, with relative saccadic amplitude equaling 31%. For the first pair, the smaller saccade was in the left eye. The following saccadic pair was not as un- 300 IM equal as the first, and relative amplitude equaled 52%. Also, the smaller saccade now appeared in the right eye. For all subjects the

- -_ l- smaller saccade always occurred opposite to the direction of the vergence movement of \ that eye, and the amount of inequality was generally larger near the start of the vergence than at the end.

& s • •• ™ r — Looking back through the responses of our "- - patients, one finds that several showed these - two characteristics. As each saccadic pair is discussed, notice that the smaller saccade m * • _ z "_- opposes the vergence movement. During the • m 1? H ft m M m first 150 msec of the vergence, the difference in the amplitudes of the two saccades was 900** fc usually greatest. In Fig. 2, a (J. K.), the saccade at the beginning of the divergence had Fig. 5. Non-Hering's law saccades in normal con- 44% of the amplitude of the fellow eye sac- trol subjects, a, Subject A. D. In left record, note 0.6° saccade in left eye and 2.0° saccade in right cade. As the saccades occurred later in the eye occurring early in convergence response. vergence, the amplitude differences were not Similar markedly unequal saccades found early in as great. In Fig. 1, b (B. N.), the saccade 600 divergence responses (right record) of same sub- msec after the start of the divergence had ject; yet observe similar size of saccades following relative amplitude of 67%. In Fig. 2, b completion of divergence, clearly demonstrating (S. H.), the smaller saccade 300 msec after that calibrations are accurate, b, Subject B. L. As the start of the divergence equaled 60% of found in Subject A. D., markedly unequal sac- the amplitude of the saccade of the other eye. cades occur during vergence response but not dur- Finally, saccades following completion of the ing fixation periods following, or prior to, the large vergence response were equal. For example, vergence responses. saccades after the convergence in Fig. 5, a, prior to the vergence in Fig. 2, a, and be- markedly unequal. For example, the saccadic tween the vergence responses in Fig. 1, b, pair 60 msec after the start of convergence in were all equal. These equal saccades occur- Fig. 5 a (A. D.), had amplitudes of 3.1° and ring after the vergences provide additional 0.8° for the right and left eyes, respectively. evidence that saccades are indeed unequal The smaller saccade measured 26% of the and are not due to a nonlinearity in the eye- amplitude of the larger saccade. The next movement recording system. saccadic pair was not as dramatically unequal. To summarize the non-Hering's law sac- Also, the smaller saccade was now in the cade result, the relative saccadic amplitudes Volume 19 Number 1 Symmetric vergence in strabismus, amblyopia 69

140

120

* 100

80- a > ft • o < 60-

< 40

O DF 6 AD 20 0 BL

J I -500 0 100 200 300 400 500 600 700 800 900 1000 START TIME (ms) OF VERGENCE Fig. 6. Relative amplitude of saccades in each eye as a function of time during vergence response for seven patients and two control subjects. Plot clearly shows reduction in non- Hering's law saccades as they occur later in the vergence movement.

Table II. Percent relative vergence Accommodative vergence Symmetric vergence targets Symmetric vergence targets along dominant eye Subject (binocular) (nondominant eye covered) (nondominant eye covered) Normal control subjects: B. L. 92.1% ± 3 26.0% ± 3 20.0% ± 5 A. D. 89.0% ± 8 17.0% ± 5 14.5% ± 9 Constant strabismus amblyopia: D. F. 16.0% ± 4 15.0% ± 3 13.0% ± 5 Intermittent strabismus without amblyopia: B. N. 7.6% ± 2 8.5% ± 4 8.0% ± 1 Amblyopia without strabismus: S. H. 7.0% ± 2 9.0% ± 1 7.5% ± 3 Former strabismus patient: J. B. 11.0% ± 5 5.3% ± 2 6.0% ± 2 from all subjects during vergence are plotted lower. Furthermore, the lowest relative in Fig. 6. The ordinate represents percent amplitudes occurred early in the vergence relative amplitude, and the abscissa is time and then slowly increased until, at about 700 before and after the start of the vergence msec, both saccades were approximately movement. The relative amplitude is defined equal. Also notice that saccades before as the ratio, in percent, of the smaller saccade the vergence movement were approximately to the larger saccade. The solid line at 100% equal; it is only during the vergence move- represents the ratio expected if equal am- ment that unequal saccades were found. The plitude saccades occurred in each eye. The plot also shows that not all saccades that oc- graph shows that most saccadic pairs during curred at a particular time after the start of vergence had relative amplitudes of 60% or the vergence were reduced by the same Invest. OphthalmoL Vis. Sci. 70 Kenyon, Ciuffreda, and Stark January 1980

1000 quence23 peak velocity-amplitude characteristics. The peak velocity-amplitude plot for saccades for normals is represented by the solid line in Fig. 7. The cluster of symbols around the normal saccadic line indicates that our patients' saccades during vergence movements had normal dynamics.

Discussion Absence of disparity vergence. Normal disparity vergence eye movements, induced by fixating near and far midline targets, are characterized by smooth, equal, disjunctive movements of both eyes. The eye movements of our control subject (Fig. 1, a) illus- trate this characteristic response, well-known in the literature on vergence eye movements.14"18 In contrast, under binocular viewing conditions where disparity vergence should be operating, most patients displayed ai 100 a conspicuous lack of normal disparity ver- MAGNITUDE (DEG gence movements. A qualitative comparison of the responses of the patients and the con- Fig. 7. Main sequence for eye movements used to identify normal saccades. The solid line represents trol subjects supports this hypothesis. locus of points for normal saccades. Symbols rep- Possible mechanisms blocking disparity resent saccades from normal subjects and Patients vergence. The absence of disparity vergence J. K. and B. N., during the vergence. The circles, under binocular viewing conditions indicates squares, and triangles represent Control Subject that a disparity blocking mechanism is oper- B. L. and Patients J. K. and B. N., respectively. ating in all groups of patients. Suppression is Saccades cluster around the main sequence line, the most likely condition. Strabismus pa- indicating that despite the inequality of the sac- tients with deviations greater than 10 PD, as cades they remain normal. found in many of our patients, generally use suppression to eliminate diplopia and confu- amount. Some of these differences were due sion caused by the strabismus.24"28 The size to intersubject variability, as can be seen by of the suppression scotoma has been found to the placement of the different symbols on the be a function of the angle of deviation, en- graph. Still, some intrasubject variability was compassing the region between and includ- evident when data from an individual subject ing the fovea and the diplopia point.24' 25 were examined. Despite this scatter, the sac- Suppression is also commonly found in pa- cades were clearly unequal during the ver- tients with amblyopia only and may explain gence in both subjects and patients. Al- the lack of disparity vergence found in some though the gradual increases in saccadic of our amblyopic patients. Of particular inequality have been plotted as a function of terest is the intermittent nature of the ver- the timing between the saccade and vergence recorded in patients having amblyopia gence, it may also be related to the velocity without strabismus. For example, Patient of the ongoing vergence and the saccade. S. H. at times made normal disparity ver- Further experiments will be needed to clarify gence, and L. T. always did so. These results, this relationship. together with the absence of normal disparity An analysis of these unequal saccades re- vergence eye movements in strabismus pa- veals that they all have normal main se- tients with and without amblyopia, suggest Volume 19 Number 1 Symmetric vergence in strabismus, amblyopia 71

that strabismus has a stronger effect on If, in the future, animal experiments involv- the disparity vergence system than does am- ing induced strabismus and/or amblyopia blyopia. vergence eye movements were measured, Some of our patients with strabismus also this would provide an additional criterion for had ARC. Interestingly, these patients also their being adequate models of human stra- showed an absence of disparity vergence. bismus and amblyopia and would also corre- Jampolsky25 showed that suppression charac- late these hypotheses with neurophysiologi- teristics are dependent on stimuli conditions, cal experiments. 28 whereas the results of Bagolini suggest that Accommodative vergence. Several pieces when patients with ARC are allowed to view of evidence strongly suggest that these un- freely, the suppression found is usually min- equal vergence responses found in our pa- 29 imal. Bagolini has established, by measur- tients are not disparity vergence but rather ing haplopia horopters, a markedly increased accommodative vergence. Accommodative Panum's area in such patients. Indeed, plas- vergence studies on normal subjects show an ticity of Panum's area in normal subjects is asymmetry in the amplitudes of the vergence dependent upon the nature of the stimuli and in each eye. Miiller19 first described the large the state of the feedback control system, as vergence in the covered eye, and we9 have has been demonstrated by Fender and Ju- recently shown that the viewing eye verges 30 31 lesz and Diner. Perhaps an expanded approximately 12% of the amplitude mea- Panum's area could eliminate the need for sured in the covered eye. The responses of vergence and thereby provide a possible Control Subject A. D. (Fig. 4, a) demonstrate mechanism underlying the absence of dis- this characteristic accommodative vergence parity vergence in our patients with ARC. movement. Similar characteristics are also For our patients J. B. and J. W. who have a found in the binocular viewing response of history of strabismus, and B. W. who has a our patients indicating that these unequal history of amblyopia, the lack of disparity vergence movements are accommodative ver- vergence movements suggests some connec- gence. A test of this hypothesis, performed tion between their former abnormal clinical by covering the patient's nondominant eye, condition and their vergence responses. showed that the response under monocu- Here, the important studies of single cortical lar conditions contained the same general units in animals with experimental strabis- characteristics as found in these same pa- mus and amblyopia may provide important tients under binocular viewing conditions. clues toward the understanding of human Furthermore, when one eye of a normal sub- strabismus and amblyopia. These reports ject was occluded, responses were similar to show that if strabismus and amblyopia are those of patients under binocular viewing produced early in life, the number of cortical conditions. Finally, the accommodative ver- cells that respond to disparity or binocular gence responses of our patients showed nor- stimuli is much less than that usually found in mal characteristics similar to the characteris- normal animals.32"36 If this abnormal visual tics of our control subjects. Table II summa- experience is continued throughout the ani- rizes the relation between the vergence mal's "sensitive period," the response pat- amplitudes in each eye for control subjects terns of the cortical cells are difficult to mod- and one patient from each category under ify later.37 Perhaps, in the case of our Patients binocular and monocular conditions. There is J. B., J. W., and B. W., their abnormal early a clear difference in the relative amplitudes visual experince may have affected cells that during binocular conditions between the con- respond to disparity to such an extent that trol subjects and the patients. Under mon- these cells no longer respond normally to ocular conditions, the controls show a large disparity information. This also may be an difference between the monocular and the additional mechanism operating in patients binocular condition, but patients show little who still have strabismus and/or amblyopia. difference in relative vergence under each Invest. Ophthalmol. Vis. Sri. 72 Kenyon, Ciuffreda, and Stark January 1980

condition. Also the relative vergences under The inequalities of these saccades are not both monocular and binocular conditions for restricted to patients,9' 39 since non-Hering's patients are similar to those of the controls law saccades appear during vergence move- under monocular conditions. Therefore we ments in normals (Fig. 5). In control sub- conclude that patients in our study made jects, the saccades occur sparsely under bin- normal accommodative vergence and not ocular conditions, usually during divergence. disparity vergence under binocular viewing In patients, the saccades are present in al- conditions. Blake et al.38 speculated that con- most all vergences. Only when the control vergence changes observed in his kittens subjects occlude one eye does the saccade reared with alternating monocular occlusion occur with the regularity of that found in pa- might be due to binocular disparity, changes tients. In the control subjects, the saccades in image size, or changes in accommodation; are due to the monocular retinal error in the in our human subjects we find that accommo- viewing eye. The occurrence of a similar dative vergence is the principal mechanism function in most patients may be construed as responsible for the vergence movement. evidence for suppression of the nondominant Non-Hering's law saccades. One of the eye in these patients. most interesting new findings of our study Possible mechanisms for non—Hering's law was the presence of non-Hering's law sac- saccades. Knowledge of the fine structure of cades during vergence. Non-Hering's law saccades may provide a clue to the underly- saccades were present in at least 85% of the ing physiological mechanism responsible for vergence movements found in all diagnostic production of unequal saccades. We have groups of patients. We were alerted to this ruled out simple linear summation of the sac- possibility because of our previous finding of cade with the vergence movement. If simple non-Hering's law saccades during accomo- linear summation of saccadic and vergence dative vergence in normal subjects.9 As positions were responsible for a change in the pointed out in Results, the smaller saccade saccadic magnitudes, then the amplitude dif- opposed direction of the ongoing vergence; ferences should be equal to the additional the direction of the saccades is determined vergence amplitude the eye moved during by the retinal error in the dominant eye. The the saccade. Compensating the saccadic am- properties of a smaller saccade opposing the plitudes for the vergence during the saccade vergence and a smaller vergence in the dom- should yield equal saccadic pairs. However, inant eye combine, so that the inequalities saccades compensated for the vergence contribute to the amplitudes of the ongoing movement still have amplitudes that are 70% convergence or divergence. For example, in of their uncompensated value. This small re- response to convergence stimuli, a patient duction is due to the short duration of the with strabismus of the left eye will use a sac- saccade, circa 25 msec, and the slow velocity cade to place the dominant right eye onto the of the vergence, circa 20°/sec. The combina- near target. A leftward saccade in both eyes tion results in little additional eye move- will move the right eye on the target and the ment. In addition, we chose to analyze sac- left eye away from the target. The smaller cades that are large enough so that the saccade opposing the vergence causes the left amount of additional amplitude due to the eye to move less than the right; the result is vergence is insignificant. that both eyes are converged more after the Nonlinear summation in the muscle or saccade than before. The addition of a larger in the motoneuronal pool is possible but vergence in the left eye than the right keeps unlikely, since the smaller saccades have the dominant right eye on the target while shorter duration than the larger saccades oc- moving the left eye towards the target. Thus curring concomitantly in the other eye and the saccade carries about half the burden of thus may be already programmed to be the vergence movement, and the accom- smaller at a higher interneuronal level. Al- modative vergence does the other half. ternatively, it may be a complex interaction Volume 19 Number 1 Symmetric vergence in strabismus, amhlyopia 73

of muscle forces, viscosities, elasticities, ac- tungsgemunschaft bei Schielenden, Graefes Arch. celerations, velocities, and positions sepa- Ophthalmol. 51:256, 1900; cited in Burian and von Noorden.' rately controlled or influenced by vergence 5. Hallden, U.: Fusional phenomena in anomalous cor- and saccadic neural control signals. In addi- respondence, Acta Ophthalmol. 37(suppl. 1): 1952. tion, the main sequence analysis shows that 6. Mariani, G., and Pasino, L.: Variations in the angle these saccades are not abnormally fast or slow of anomaly and fusional movements in cases of small with respect to saccades made free from ver- angle convergent strabismus with harmonious anomalous correspondence, Br. J. Ophthalmol. 48:439, gence influences. The peak velocity and am- 1974. plitudes correspond well with the normal 7. Kretschemer, S.: La fausse correspondence remain sequence measurements. Therefore any tinienne, Doc. Ophthalmol. 9:46, 1955; cited in mechanism which will reduce or enhance Burian and von Noorden.' these saccades must equally affect the peak 8. Stark, L., Vossious, G., and Young, L.: Predictive velocity as well as the amplitude. Further control of eye tracking movements, IRE Trans. Human Fac. Electr., HFE-3:52, Sept., 1962. experimental, simulation, and neurological 9. Kenyon, R.V., Ciuffreda, K.J., and Stark, L.: Bin- studies will be necessary to clarify the gen- ocular eye movements during accommodative ver- eration of the non-Hering's law saccades. gence, Vision Res. 18:545, 1978. Summary. Vergence eye movements in 10. Krishnan, V.V., and Stark, L.: A heuristic model for the human vergence eye movement system, IEEE most patients with strabismus and/or am- Trans. Biomed. Eng., BME-24 1:44, 1977. blyopia are restricted to accommodative ver- 11. Fry, G.A., and Hill, W.W.: The center of rotation of gence movements. The characteristic re- the eye, Am. J. Optom. Arch. Am. Acad. Optom. sponse to disparity produced by targets at dif- 39:581, 1962. ferent distances involves binolcular saccades 12. Ciuffreda, K.J., Kenyon, R.V., and Stark, L.: Ab- normal saccadic substitution during small-amplitude which fixate the dominant eye on the target pursuit tracking in amblyopic eyes, INVEST. OPH- together with an accommodative vergence. THALMOL. VISUAL SCI. 18:506, 1979. Saccades of both patients and control subjects 13. Griffin, J.E.: Binocular anomalies: Procedures for that occur during vergence are unequal, with Vision Therapy, Chicago, 1976, Professional Press the saccade moving against vergence being Inc., pp. 74-75, 95-96. 14. Westheimer, G., and Mitchell, A.M.: Eye move- the smaller. Main sequence analysis shows ment responses to convergent stimuli, Arch Oph- that both equal and unequal saccades have thalmol. 55:848, 1956. normal peak velocity-magnitude relation- 15. Riggs, L.A., and Niehl, E.W.: Eye movements re- ship. Strabismus appears to have a stronger corded during convergence and divergence, J. Opt. disruptive effect on normal disparity ver- Soc. Am. 50:913, 1960. 16. Rashbass, C., and Westheimer, G.: Disjunctive eye gence than does amblyopia; surgery and or- movements, J. Physiol. 159:339, 1961. thoptics to relieve strabismus and amblyopia 17. Zuber, B.L., and Stark, L.: Dynamical characteris- have mixed effects on vergence responses. tics of fusional vergence eye-movement system, IEEE Trans. System Sci. Cyb., SSC 4 1:72, 1968. We are grateful to Dr. Kenneth Poise, Clinic Direc- 18. Westheimer, G., and Mitchell, D.: Sensory stimu- tor, and Dr. J. David Grisham for their assistance in lus for disjunctive eye movements, Vision Res. obtaining patients for this study. We also thank Dr. Allan 9:749, 1969. N. Freid for his helpful suggestions. 19. Miiller, J.: Elements of Physiology, trans, by W. Baly, London, 1843, Taylor & Walton, vol. 2, REFERENCES pp. 1147-1148. 1. Burian, H.M., and von Noorden, G.K.: Binocular 20. Ciuffreda, K.J., Kenyon, R.V., and Stark, L.: Pro- Vision and Ocular Motility, St. Louis, 1974, The cessing delays in amblyopic eyes: evidence from C. V. Mosby Co. saccadic latencies, Am. J. Optom. Physiol. Opt. 2. Burian, H.M.: Fusional movements in permanent 55:187, 1978. strabismus; a study of the role of central and periph- 21. Ciuffreda, K.J., Kenyon, R.V., and Stark, L.: In- eral retinal regions in the act of binocular vision in creased saccadic latencies in amblyopic eyes, IN- squint, Arch. Ophthalmol. 26:626, 1941. VEST. OPHTHALMOL. VISUAL SCI. 17:697, 1978. 3. Bielschowsky, A.: Untersuchungen iiber das Sehen 22. Ciuffreda, K.J., Kenyon, R.V., and Stark, L.: Dif- der Schielender, Graefes Arch. Ophthalmol. 50: ferent rates of functional recovery of eye movements 406, 1900; cited in Burian and von Noorden.' during orthoptics treatment in an adult amblyope, 4. Schlodtmann, W.: Studien iiber anomale Sehrich- INVEST. OPHTHALMOL. VISUAL SCI. 18:213, 1979. Invest. Ophthalmol. Vis. Sri. 74 Kenyon, Ciuffreda, and Stark January 1980

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