OW-6989/92 %.5.00+ 0.00 Copyright 0 1992 Pergamon Press pie

Vision Res. Vol. 32, No. 3, pp. 489497, 1992 Printed in Great Britain. All rights reserved

Disconjugate Ocular Motor Adaptation in Rhesus Monkey AKIHIKO

OOHIRA,*t

DAVID S. ZEE*

Received 28 March 1991; in revised form 26 July 1991

We report a rno~ifar inducing d~s~onjugate, orbital-position ~pendent, ocuiur motor adaptai~o~ in the rhesus monkey. Animals wore a combination of laterally-displacing prisms placed in front of one eye calling for a discrete change in ocular alignment when the eyes reachedparticular orbital positions. After wearing the prism combination the animals developed adaptive changes both in static alignment during$xation and in dynamic alignment during eye movements. These changes persisted with only one eye viewing and so became independent of the immediate presence of disparity cues. There were, however, imperfections in the adaptive responses; the changes in the innervation were gradual across the prism edge, not abrupt as required. ThisJinding may reflect inherent limitations in the capability for disconjugate adaptation.

Eye movements Monkey

Saccades

Vergence

Prism

displacing prisms, of different orientations (base-in or base-out), strengths, and sizes, placed in front of one eye, to elicit a change in ocular alignment as a function of orbital position. When a normal animal wears spectacles for anisometropic correction, it shah suffer from the difference in image size and in accommodation between the two eyes. Prisms can give retinal disparity without these troublesome effects. Con~rning retinal disparity, however, this optical combination differs from spectacles used to correct anisometropia in one important aspect. At orbital positions corresponding to the prism edges a discrete rather than a gradual change in relative innervation is called for, and not further change in relative alignment is called for until another prism edge is reached. Some of the results have been presented in preliminary form (Oohira & Zee, 1992).

INTRODUCTION

Much research has been focused upon the mechanisms by which the central nervous system calibrates eye movements for optimal visual-oculomotor performance. Most earlier studies have been concerned with adaptive control of conjugate ocular motor mechanisms though more recent studies have turned to mechanisms of discon~ugate ocular motor adaptation, i.e. adjustments of the relative innervation to the two eyes to ensure optimal binocular visual-oculomotor performance (Henson & Dharamshi, 1982; Viirre, Cadera & Vilis, 1988; Erkelens, Collewijn & Steinman, 1989a; Zee & Levi, 1989; Schor, Gleason & Horner, 1990; Oohira, Zee & Guyton, 1991). One model for the investigation of disconjugate ocular motor adaptation is spectacle-corrected anisometropia. Because of the prismatic effect (rotational magnification) of the corrective lenses away from their optical centers, a retinal disparity occurs for targets that appear away from fixation. Accordingly, if binocular fixation is to be immediate when the eyes reach the new location of the target, the central nervous system must readjust ocular alignment during every conjugate change in gaze. This is exactly what happens in humans who wear a spectacle correction for anisometropia (Zee et al., 1989; Erkelens et al., 1989a; Oohira et al., 1991). Here, we report an animal model to study disconjugate adaptation. We used a combination of laterally*Departments of Neurology and Ophthalmology, The Johns Hopkins University School of Medicine, Baltimore, MD 212OS, U.S.A. tTo whom all correspondence and reprint requests should be addressed at: Akihiko Oohira, Department of Ophthalmolo~, University of Tokyo School of Medicine, 7-7-3 Hongo, Bunkyo-ku, Tokyo 113, Japan.

Adaptation

generic

procedures and eye movement rewording

Three juvenile (2.5-3.5 yr-old) rhesus monkeys were used in this study. Under general anesthesia, a headplate of acrylic was attached to the skull of each monkey and a coil of wire was sutured to the sclera of each eye (after Judge, Richmond & Chu, 1980). Transparent plexiglass “goggles” were attached to the head plate so that laterally-displacing membrane prisms could be adhered to the plexiglass I cm in front of the left eye. The plexiglass and the prisms were trimmed so as not to directly touch the nose and cheek. Vertical size of the prisms was almost large enough to cover a11visual field of the monkey. The prisms extended horizontally from the middle of the face to 0.5 cm lateral to the side of the

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face. During testing the head was immobilized by fixing the head plate to the primate chair. Movements of both eyes were measured using the magnetic-field search-coil technique (Robinson, 1963) and sampled by digital computer at 500 Hz. The vergence angle was computed from the difference between the position of the right and left eye. Monkeys were trained to fixate and to follow targets by reinforcing good performance with a liquid reward. All recordings were carried out in a dimly illuminated room except for spontaneous saccades and vestibulo-ocular responses which were measured in total darkness. During the non-testing time the monkeys were kept in a cage without any physical restraint. Stimulus presentation Saccades and fixation were tested by having the monkey refixate between stationary light-emitting diodes (LEDs) located horizontally and vertically across the visual field, at 2.5 deg intervals. The distance from the eyes to the center target was 186 cm. Smooth pursuit was elicited with a square-shaped light source (subtending 1.6 deg), rear-projected onto a translucent, featureless, screen located 61 cm in front of the monkey. This target required the animals to converge 1.9 deg more than when compared with the case of looking at the LED 186 cm from the head. The wave form of target motion was step-ramp designed to eliminate the need for a catch-up saccade. Vestibulo-ocular responses were recorded in total darkness during a constant velocity (30 deg/sec) rotation of the animal chair.

FIGURE 1. Schematic diagram of a 24-2 prism combination in front of a monkey’s left eye. This combination leaves the central I5 deg unchanged (ex. Target A is unchanged) but displaces temporal and nasal images centripetally (ex. Target B is displaced to B’) by 2 prism diopters. This calls for relative divergence on right gaze and relative convergence on left gaze.

all the data that are presented were obtained monocular (right eye) viewing conditions.

under

Data analysis Prism arrangement Two prism combinations were used in this experiment so that images from the temporal, the central 15 deg, and the nasal fields could be displaced by different amounts. The prisms were always placed in front of the left eye. The first combination was a 2A base-out prism in the temporal field, no prism in the central field and a 2A base-in prism in the nasal field (denoted 2-O-2). The monkey would have to diverge by 2A (about 1.1 deg) when looking beyond 7.5 deg to the right and to converge by 2A when looking beyond 7.5 deg to the left (Fig. 1). The second combination was a jA base-out prism in the temporal field, 2* base-out prism in the center field and 2* base-in prism in the nasal field (denoted 5-2-2). In either case, when a change in position of the left eye caused its line of sight to pass through a portion of the plexiglass containing a different prismatic correction, the amount by which the left eye had to rotate was always less than that of the right eye. Measurements were made before and after 1-15 days of wearing the 2-O-2 prism combination. Then, the prism combination was changed to 5-2-2 and measurements were repeated l-15 days later. Calibration data of eye position for each eye was obtained each testing day by having the monkey fixate each LED without prisms with the other eye occluded. The polynomial fitting function was applied to the calibration data to linearize the data obtained on each day. Unless otherwise stated

Eye movement data were analyzed off-line. Individual trials were displayed on a video monitor and the eye movement traces were marked as follows; an “i” identifies the position of the eye at the beginning of the saccade (when eye velocity exceeded 20 deg/sec), A “p” identifies the position of the eye at the end of the rapid (pulse) portion of the saccade (eye velocity < 30 deg/sec) (see Figs 2 and 3). A vergence trace was also displayed by subtracting the calibrated right and left eye position signals. The static alignment (phoria) was obtained by subtracting the left eye position from the right eye position when the animal was fixating the target with the right eye (left eye occluded). The measurement was made from the position of the eyes just prior to the onset of the saccade (“i”) to the next target. The phoria was measured when viewing targets placed at 2.5 deg intervals between + 15 deg and also at targets placed at f 20 deg. For each target position an average of at least 7 measurements was calculated. The change in phoria at each target position after adapting to the prism combinations was calculated by subtracting the average phoria data obtained before adaptation from that obtained after adaptation. Student’s t-test was used to examine the statistical significance of this change. The change in dynamic (intrasaccadic) alignment was calculated by subtracting the amplitude of the rapid portion of the saccade (“p” - “i”) of the left eye from that of the right eye. For this purpose saccades were

DISCONJUGATE

OCULAR

MOTOR ADAPTATION

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Post

Pre

Verg

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0.50

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Time (set) FIGURE 2. Recording of a saccadic eye movement from center to right 10 deg before (Pre) and after (Post) 15 days of wearing a 5-2-2 prism combination. Monkey T. For these records the right eye is viewing and the left eye is occluded. In this case the prisms require 4 prism diopters (about 2.3 deg) of divergence when the eyes refixate from center to right 10 deg. Before adaptation there is a transient divergence during the saccade. After adaptation, the eyes diverged 1.6 deg and remained so during and after the saccade. The eye positions in this right panel are slightly more esophoric than average. Right eye position (R), left eye position (L) and vergence angle (Verg) are shown. Divergence is positive. On the eye position traces, ‘7” is the position of the eye at the beginning of the saccade, “p” is the position at the end of the rapid (pulse) portion of the saccade. On the vergence trace, “i” and “p” are the vergence angle at the beginning and at the end of the pulse portion of the saccade.

elicited to target displacements of 5-30 deg. The average value of at least 5 saccades of each type was calculated. The adaptive change in dynamic alignment was calculated by subtracting the average intrasaccadic alignment change before adaptation from that after adaptation. Student’s t-test was used to examine the statistical significance of this change. RESULTS

General features of the adaptive response

Figures 2 and 3 show individual eye movement records from one of the animals (monkey T) before and after wearing the 5-2-2 prism combination for 11 days. In this case the targets were located at center and right 10 deg, which called for alignment changes of about 2.3 deg divergence, for rightward saccades (Fig. 2) and 2.3 deg

2

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convergence, for leftward saccades (Fig. 3). Viewing during testing was monocular so that no disparity cues were available. Note that in the pre-adaptation state (left-hand panels) there was a transient divergence during both rightward and leftward saccades. After wearing the prism combination the monkey showed a considerably different pattern of change in intrasaccadic alignment (right-hand panels). The changes can be particularly well seen in the vergence traces. For rightward saccades, the eyes now diverged during the saccade and remained so. For leftward saccades, the eyes initially diverged but then converged by considerably more and continued to converge slowly. Thus, after wearing the prism combination there were changes both in dynamic alignment, i.e. in the relative positions of the two eyes during saccades, and in static alignment, i.e. the relative position of the eyes during monocular fixation (phoria).

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FIGURE 3. Recording of a saccadic eye movement from right 10 deg to center before (Pre) and after (Post) 15 days of wearing a 5-2-2 prism combination. Monkey T. The viewing conditions, conventions and abbreviations are the same as in Fig. 2. Before adaptation there is a transient divergence during the saccade. After adaptation of the eyes, after a small divergence, converges 0.6deg during the saccade and continue to converge slowly after the saccade.

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amount fell to zero as the eyes moved further to the left (Fig. 4 bottom panel, monkey T). As a control, the vertical alignment of both eyes was measured during right eye viewing in two monkeys after the animals had adapted to the 5-2-2 prism combinations. No change in vertical alignment was found when compared with the pre-adaptation data. Changes in dynamic alignment Top and middle panels of Fig. 5 summarizes the adaptive changes in dynamic (intrasaccadic) alignment

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Monkey B

-

Monkey M

-3

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Monkey T

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FIGURE 4. Adaptive change in static alignment (phoria) after 414 days of wearing the 2U2 (top panel) or the 5-2-2 (bottom panel) prism combination. The adaptive changes in phoria were in a direction appropriate to the demands of the prisms (the dashed horizontal lines). However, despite the abrupt change called for by the prism combination at right and left 7Sdeg, the change in phoria was gradual. Monkey T did not adapt to the SA prism and as the position of the eyes was shifted beyond left 7.5 deg, the change in phoria gradually returned to zero. Each point respresents the difference between the average value of at least 7 measurements on the day of pre-adaptation and that of post-adaptation. These differences were statistically significant (P -c0.05) except for several points, where the phoria changes were within kO.3 deg.

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Changes in static alignment Figure 4 summarizes the adaptive changes in static alignment or phoria [ocular alignment with one eye (the right eye) viewing], for each monkey, after wearing the 2X%2 (top panel) and 5-2-2 (bottom panel) prism combination. Plotted (phoria change) is the difference between the average value of the phoria before and the average value after adaptation to the prism. These differences were statistically significant (P < 0.05) except for several points, where phoria change was within + 0.3 deg. The degree of adaptation of the phoria varied as a function of orbital position. The phoria change was gradual across the visual field, not abrupt as the prism combination required (dashed lines) and there was even some adaptive change where there should have been none (e.g. the center visual field with the 2-O-2 prism; top panel Fig. 4). Nevertheless, the phoria change did follow roughly the power of the prisms, One monkey did not adapt to the 5a prism. During binocular viewing, this animal fixed upon the target with both eyes when the target was center or in the right visual field, but only with its left eye when the target was in the far left visual field (the portion of the visual field covered by the 5a prism). Even so, the phoria in positions of gaze beyond left 7.5 deg showed some adaptive response, though the

0 -1 -2 -3 -4

conv

L15-R15

LlO-RlO

L5-R5

LlO-0

Saccade

m

Actual

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Predictedtphoria)

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O-R10

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O-R15

Type Required(prism)

FIGURE 5. The adaptive change in dynamic (intrasaccadic) alignment after 4 days of wearing the 2-O-2 (top panel), and after 5 days of wearing the S-2-2 (middle panel) prism combinations in front of the left eye, for monkey B. Bottom panel is the adaptive change after 15 days of wearing 5-2-2 prism combination for monkey T. Hatched bars depict the difference between the average value of intrasaccadic vergence before and the average value after adaptation. Solid bars indicate the required vergence changes based upon the prism combination. Open bars are predicted vergence changes calculated from the phoria change (Fig. 4). Vergence change is plotted against each type of saccade; for example, saccade type LlO-0 is saccade from left 10 deg to center in the upper row (rightward saccade) and center to left 10 deg in the lower row (leftward saccade), in each panel. If the vergence change was in the opposite direction to that required by the prism, it is depicted in the opposite row, as is found in leftward saccades of type Ll5-0 (second stippled bar and open bars) in the bottom panel. These adaptive changes (stippled bars) are statistically significant (P < 0.05) except for one value in the bottom panel (*).

DISCONJUGATE

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MOTOR ADAPTATION

the 2-O-2 (top) and the 5-2-2 (middle) prism combination in monkey B. The difference between the average value of intrasaccadic vergence before, and the average value after adaptation is plotted in relationship to saccade size and direction. This difference was statistically significant (P < 0.05) in every type of saccade. This adaptive change in dynamic alignment largely paralleled the predicted value (open bars in Fig. 5) calculated from the change in phoria shown in Fig. 4. The data show that fairly good amount of the adaptive change in alignment occurred during the saccade itself. The adaptive change in intrasaccadic alignment during right or leftward saccades beginning from the center were larger for the 15 deg than for the 10 deg displacements even though the change in intrasaccadic alignment called for by the prism was the same. The adaptive change in intrasaccadic alignment for rightward (calling for divergence) saccades was usually larger than that for leftward (calling for convergence) saccades. There was also some (mal)adaptive change in intrasaccadic alignment during the saccades between right and left 5 deg targets, in which case there should have been none. Even with both eyes viewing, this inappropriate change in intrasaccadic alignment occurred during saccades elicited between right and left 5 deg targets, and had to be corrected by a fusional movement beginning several hundred milliseconds after the saccade. The results in monkeys M and T were similar to those for monkey B except for monkey T who did not adapt to the 5A prism (in the left field) of the 5-2-2 combination. Saccades to and from targets in the left field, covered with the 5A prism, showed little intrasaccadic vergence change (bottom panel of Fig. 5, LlO-0, L15-0). However, also in this animal, these changes in dynamic alignment largely paralleled the predicted value (open bar in the bottom panel of Fig. 5) calculated from the change in phoria (Fig. 4). These adaptive changes in intrasaccadic alignment measured with monocular (right eye) viewing above mentioned was almost the same as that measured with both eye viewing (Fig. 6). The monkeys also showed a small change in the amount of postsaccadic vergence. For leftward saccades (convergence was required), the eyes continued to converge after each saccade as is shown in Fig. 3 (right). The amount of postsaccadic alignment change after rightward saccades (divergence was required) was smaller and sometimes in the wrong direction.

div

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Saccade m

ActualCREW

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L15-0

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Type

Required(prism)

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ActualfBEV)

FIGURE 6. The adaptive change in dynamic (intrasaccadic) alignment 5 days (top panel, monkey B) or 15 days (bottom panel, monkey T) after wearing the 5-2-2 prism combination. Solid bars indicate the required changes based upon the prism combination. Stippled (right eye viewing; REV) and open bars (both eye viewing; BEV) depict the difference between the average value of intrasaccadic vergence before adaptation and the average value after adaptation. Except for the pattern within the bars the conventions am similar to these described in the legend of the Fig. 5. The adaptive change measured with BEV was almost the same as that measured with REV. These adaptive changes are statistically significant (P < 0.05) except for three values in the bottom panel (*). The open bar for R15-L15 leftward saccade in top panel is not shown because of small number of saccades obtained.

wearing the 5-2-2 combination (Fig. 7). The changes in static (phoria) alignment over time (Fig. 8) roughly paralleled those for dynamic alignment. There was considerable adaptation within 24 hr after wearing each prism combination, and the adaptation continued to

Time course of alignment change The time course of adaptive change in static and dynamic ocular alignment was examined in monkey M. When wearing the 2-O-2 prism combination there was considerable adaptive response in dynamic (intrasaccadic) alignment within 24 hr (Fig. 7) which did not change further over the next 4 days. When the 220-2 prism combination was replaced by a 52-2 prism combination there was again considerable change in alignment within 24 hr, but in most instances, further adaptation continued to occur even up to 8 days after

-

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L-2-2 -

prism

20 day

AZ

o-w5

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Saccade

Type

LlocO

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FIGURE 7. Time course of dynamic adaptive change in ocular alignment. Monkey M. The dynamic (intrasaccadic) change is shown as the difference between the average value of intrasaccadic vergence before (day 0) and the average value after adaptation at each day for each type of saccade. There was considerable intrasaccadic change after wearing each prism combination for just 1 day, although adaptation continued to increase after that.

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position adaptive ing, i.e. presence

S. ZEE

of the eyes within the orbit. Once learned, these responses appear during the monocular viewthey become independent of any immediate of disparity cues.

Optical combinations to induce disconjugate adaptation

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-

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FIGURE 8. Time course of static adaptive change in ocular alignment. Monkey M. The data of “I day before” is taken when the monkey has been wearing the 242 prism combination for 4 days, i.e. 1 day before replacing the prisms with the 5-2-2 prism combination. The slope of the curves became steeper, indicating better adaptation, as the time of prism exposure increased.

increase even up to 14 days after wearing the 5-2-2 prism combination. Ocular alignment change during pursuit, nystagmus and saccades in the dark

z)estibular

We also examined changes in ocular alignment during pursuit (Fig. 9, left), vestibular nystagmus in darkness (Fig. 9, middle) and spontaneous saccades in darkness (Fig. 9, right) in monkey M. As for visually guided saccades, adaptive changes in ocular alignment occurred as a function of orbital position and the dynamic change during these movements closely paralleled those expected from the adaptive change in phoria. DISCUSSION

The main result of this study is that monkeys have a capability for “disconjugate”, adaptation to visual conditions that call for each eye to rotate by a different amount. Furthermore, the amplitude and the direction of the “disconjugate” adaptation can be tailored to the

The optical means that we used to produce the visual conditions necessary for disconjugate ocular motor adaptation were similar to the spectacles used to correct for naturally-occurring anisometropia in human beings. In the latter case, the eye viewing through the lens with the more minus correction must rotate less than the other eye. The prism combination we used was similar to a correction for anisometropia in which the spectacle in front of the left eye was relatively minus compared to that for the right eye. There are, however, important differences between the two optical paradigms, which probably influenced our results, The amplitude of the rotational magnification factor of a spherical lens, due to its prismatic effect, is constant so that disparity increases gradually, and roughly linearly with eccentricity. Laterally-displacing prisms, however, produce a changing rotational magnification factor that is a function of the strength, orientation, and location of the prism. Thus, with a spectacle correction for anisometropia, the amount of relative convergence or divergence called for varies gradually as a direct function of the position of the eyes in the orbit. In contrast, with the laterally-displacing prisms, the amount of relative convergence or divergence is constant when the eye is in any position in the orbit in which its line of sight passes through the same prism. When the line of sight is rotated to pass through a different prism, however, the amount of relative convergence or divergence changes abruptly, to a new level commensurate to that prism. Thus, one would predict a smooth, gradual adaptive change in ocular (static) alignment with spectacles correcting for anisometropia and a more abrupt change in ocular alignment with the combination of laterally-displacing prisms.

1

R

FIGURE 9. Recordings of smooth pursuit (left), vestibulo-ocular response (middle) and spontaneous saccades (right) in monkey M after 13 days of wearing 5-2-2 prism combination. The latter two were recorded in total darkness with both eye viewing. Right eye (R), left eye (L), vergence angle (Verg) and predicted vergence angle (Pred) calculated from the phoria data on the 14th day is shown. Note the similarities between “Verg” and “Pred” in all 3 recordings. Chair speed is 30 deg/sec. Traces of “Verg” and “Pred” are shifted downward in this figure for clarity.

DISCONJUGATE

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Likewise, for dynamic changes in alignment, a spectacle correction for anisometropia calls for the ratio between the change in ocular alignment and the amplitude of rotation of the eyes, to be roughly constant. So, for example, if a 2 deg change in relative alignment must accompany a 10 deg saccade, a 4deg change in alignment must accompany a 20 deg saccade. For the prism combination that we used in our experiments, however, the ratio between the change in ocular alignment and the amplitude of rotation of the eyes is not constant but varies gradually with eye rotation, as long as the line of sight of that eye passes through the same prism. Once the line of sight is rotated to a new prism, though, the ratio changes abruptly to a new level, and then gradually again as the eyes continues to rotate, but still passing through the same prism. Thus, one would predict that the adaptive change in intrasaccadic (dynamic) alignment with a spectacle correction for anisometropia would be linearly related to the amplitude of the change in the position of the eyes in the orbit. With the prism combination, however, one would predict that the adaptive change in intrasa~adic alignment would only change, and then abruptly, when the line of sight was moved from one prism to another. Finally, at the prism edge there is a small “blind spot” (1-2 deg, depending on the prism size) for the eye viewing through the prism. This might lead to some variability in the amount of retinal disparity when the line of sight was pointed near, or at, the prism edge. These abrupt changes of retinal disparity might have been annoying to the monkeys. They could avoid this trouble by looking only through the center or right (left) field, or by ignoring the diplopia instead of fusing the images. With the head free in the cage, it is difficult to look continuously through the specific field, because vestibulo-ocular reflex or reflexive saccades shall bring the eyes into other fields. Retinal disparity by 5* baseout prism (requires 3 deg convergence) is well within the fusional ability of normal monkey (Boltz & Harwerth, 1979). In spite of this, monkey T did not adapt to the P prism and apparently saw diplopia in the left field. During the learniag time in the cage this animal might have ignored the diplopia in the left field because the animal often watched one of the authors through the P prism without turning his head to the left to avoid the diplopia. Comparison of desired and actual adaptive changes

The amount of adaptation of static ocular alignment shown by our monkeys reflected the particular prism combination that the animals wore but there were important discrepancies between the values of actual adaptive responses and those expected from the prism configuration. Near the edge of the prism, adaptation of the phoria was gradual, not abrupt. The small ““blind spot” created by the prism edge was unlikely to account for this phenomenon since the range of eye positions over which the phoria changed gradually was much broader than the size of the “blind spot”. In fact, the rate

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of change in phoria within the central 15 deg of vision was roughly linear, which indicates that the mechanism producing the adaptive change in phoria has a relatively low spatial frequency. Likewise, some variation in the phoria adaptation might also be expected due to the varying degrees of vergence associated with fixing upon objects located at different depths. A change in the angle of vergence could alter the amount of disparity introduced for a given position of the right eye, especially when the line of sight of the left eye was passing near one of the prism edges. The overall effect of convergence would be to shift the curves that showed the adaptation of the static alignment, to the left, so that relative divergence of the visual axis would appear at more leftward positions of the right eye. Thus, our prism combination also required phoria adaptation to be tailored to the viewing distance. Nevertheless, this effect of convergence would be small in our experiment since there was no change in the strength of the prism in the center 15 deg of the visual field. For convergence to alter the prism-induced disparity it would have to be very large enough to hold the eyes away from the primary position such that the line of the left eye was near a prism edge (target depth only about 11 cm from the eyes). The adaptive changes in dynamic (intrasaccadic) alignment also reflected the prism combination worn by the animals but, like the change in static alignment, was imperfect. There was an inappropriate, (mal)adaptive change in intrasaccadic vergence for saccades made within the central 15 deg of the visual field, in which no adaptation was required. For saccades that moved the line of sight from one prism to another, the change in intrasaccadic vergence was not constant, as it should have been, but increased with the size of the saccade. By and large, these adaptive changes in intrasaccadic alignment mirrored the adaptive changes in static alignment. We also observed that the adaptive changes in intrasaccadic alignment were greater for rightward (calling for relative divergence) saccades, than for leftward (calling for relative convergence) saccades. This could be related, in part, to the relative divergence that accompanies the onset of all horizontal saccades, though the inherent divergence during saccade was corrected for by subtracting the intrasaccadic vergence change after adaptation from that measured prior to adaptation. Another possible explanation for this asymmetry may be inherent limitations in the ability of disparity-induced vergence to diverge the eyes (Boltz & Harwerth, 1979). If the necessary degree of divergence is not reached during the saccade, a subsequent, disparity-induced vergence may not be able to further diverge the eyes. In contrast, if convergence is called for, and the necessary degree is not reached during the saccade, disparity-induced convergence could easily be used to correctly align the eyes after the saccade. Hence, it would be more critical to program the correct amount of intrasaccadic divergence than of convergence during disconjugate adaptation.

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Mechanisms of disconjugate adaptation of static alignment

focus since the prisms are fixed relative to the head. This implies that there must be a three~imensional reorganiTo adapt to optical conditions that produce a dis- zation of subjective visual space. The central nervous parity that varies as a function of the position of the eyes system might utilize this map to calculate the amplitude of the saccade to be made by each eye. Compatible with, in the orbit, the brain must remap the relationship between ocular alignment and the position of the eyes in but not proving this idea, the adaptive changes enthe orbit. The major stimulus to such a remapping is countered during visually-guided saccades, intrasaccadic presumably disparity and the consequent attempt to fuse alignment, smooth pursuit, vestibulo-ocular response and spontaneous saccades paralleled the adaptive the images with vergence eye movements. One animal did not fuse the images of the targets in the left visual change in static alignment. Schor et al. (1990), however, induced selective disconfield which was covered with the 5A prism. In this part of the visual field it gradually lost the adaptive change jugate adaptation for saccades or pursuit by producing in phoria that was present in the other part of the visual a vertical disparity in a haploscopic system. This result does not necessarily conflict with the interpretation of field. This fact suggests that fusion, and perhaps attempt our results. The subjects in the experiment of Schor et al. to fuse, is the main contributing factor for the adaptation. A number of other factors, however, such as were required only to fuse the images of two small accommodation, proximal vergence and the sense of targets with the head restrained. The visual scene did not contain other visual stimuli in different directions or nearness, relative size of objects, the prism-induced depths. Thus, subjects of Schor et al. did not need to distortions of visual space may be important in the remap subjective visual space, and they adapted only to remapping of ocular alignment as a function of orbital the special conditioning stimulus. position. The mechanisms underlying the adaptive changes in While our monkeys did adapt to the prisms, the intrasaccadic vergence could be related to a phenomenon adaptation was not precisely tailored to the optical that occurs during normal binocular viewing. A change combination that was used; adaptation was gradual, not in vergence is reported to be much faster if it is conjoined abrupt. We think that the most likely explanation is a limitation in the ability of the brain to program an with a saccade in normal human beings (Enright, 1984; abrupt change in the relative innervation to the two eyes Erkelens, Steinman & Collewijn, 1989b; Levi, Zee & when the position of the eyes in the orbit changes by only Hain, 1987). Accordingly, it might be possible that the a small amount. Related to this idea are the concepts of relatively rapid intrasaccadic vergence change made by adapted monkeys has a common mechanism with the spread of phoria adaptation and of phoria adaptive intrasaccadic vergence change made by unadapted monfields (Henson et al., 1982; Sethi & Henson, 1985). keys during refixating between targets that called for a The phoria adaptation that occurs in response to wearing a prism when the eyes are kept in just one combination of both a vergence and a conjugate change in gaze. The amount of each component of this combiparticular position in the orbit does spread into adjacent positions but with a gradually diminishing effect as the nation in adapted state would be determined according to the location of the targets in the remapped subjective eyes more further away from the tr~ning position. Furthermore, intermediate values of adaptation occur visual space. when the eyes are positioned between two training Functional and clinical implications positions where there are different demands for ocular While our animals showed a capability for disconjualignment. Of course, as hinted at in Figs 7 and 8, a gate adaptation in our experimental paradigm, they were longer exposure to the prisms might have led to a better not able to tailor the adaptive response precisely to the match between the prism req~rements and the adaptive requirements of the prism combinations. Nevertheless, response. the type of response shown in our experiments would meet the needs for adaptation to the usual stimulus Mechanisms of disconjugate adaptation of dynamic experienced in natural circumstances; a relatively small alignment asymmetry in the ability of yoke pairs of extraocular Finally, we asked what might be the stimuli and the muscles to rotate the globes conjugately. The correct motor mechanisms by which intrasaccadic alignment is response to such a stimulus would be a gradual change adaptively readjusted. As suggested above, disparity, in relative innervation as the eyes move across the visual and the fusional attempt to overcome it, are probably field; just what was observed in this study. the stimuli to static phoria adaptation. In the case of the Relatively small degrees of asymmetry in muscle adaptive changes in intrasaccadic alignment, the pres- strength must frequently occur as a result of corrective ence of disparity immediately after a saccade seems to be surgery for either paralytic or non-paralytic strabismus, the necessary stimulus (Erkelens et al., 1989a; Schor especially when the eyes are directed away from the et al., 1990). The remapping of static ocular alignment primary position of gaze. as a function of the position of the two eyes in the orbit Patients frequently have diplopia immediately after might be the critical change in our experiment. Furthersuch surgery but it usually diminishes in the ensuing few more, as discussed above, the orbital-position dependays or weeks. A number of factors may contribute to dence of adaptive change must vary with the depth of this improvement including mechanical changes in the

DISCONJUGATE

OCULAR

MOTOR ADAPTATION

muscle and suppression of an image from one eye. Nevertheless, the type of the disconjugate adaptation shown by our monkeys is probably also important. On the other hand, a limited ability to make large changes in relative innervation with small changes in absolute eye position may be the reason that human patients seldom achieve a wide range of binocular function when the degree of asymmetry in the strength between the muscles in a yoke pair is large (e.g. an acquired, complete lateral rectus palsy). An exception may be the congenital abduction deficit of Duane s~drome in which patients may have a considerable preservation of binocular function within the intact field of gaze. REFERENCES Boltz, R. L. & Harwerth, R. S. (1979). Fusional vergence ranges of the monkey; a behavioral study. Experimental Brain Research, 37, 87-91.

Enright, J. T. (1984). Changes in vergence mediated by saccades. Journal of Physiology, London, 350, 9-3 1. Erkelens, C. J., Collewijn, H. & Steinmann, R. M. (1989a). Asymmetrical adaptation of human saccades to anisometropia spectacles. Znvestigative ophthalmology and Visual Science, 30, 1132-114s. Erkelens, C. J., Steinman, R. M. & Coliewijn, H. (1989b). Ocular vergence under natural conditions; II. Gaze shifts between real targets differing in distance and direction. Proceedings of the Royal Society of London, B, 236, 441-465.

Henson, D. B. & Dharamshi, B. G. (1982). Oculomotor adaptation to induced heterophoria and anisometropia. Investigative Ophthalmology and Visual Science, 22, 234240.

IN RHESUS MONKEY

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Oohira, A. & Zee, D. S. (1992). Disconjugate ocular motor adaptation in rhesus monkey. In Shimazu, H. SCShinoda, Y. (Eds), Vestibufar and brain stem control of eye, head and body movements. Tokyo: Springer. In press. Oohira, A., Zee, D. S. & Guyton, D. L. (1991). Disconjugate adaptation to long-standing, large-amplitude spectacle-corrected anisometropia. Investigative Ophthalmology and Visual Science, 32, 1693-1703.

Robinson, D. A. (1963). A method of rn~su~ng eye mov~en~ using a scleral search coil in a magnetic field. IEEE transactions on Biomed~caI Engineering, BME-10,

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Schor, C. M., Gleason, J. & Horner, D. (1990). Selective nonconjugate binocular adaptation of vertical saccades and pursuits. Vision Research, 30, 1827-I 844.

Sethi, B. & Henson, D. A. (1985). Vergence-adaptive change with a prism-induced noncomitant disparity. American Journal of Optometry and Physiological Optics, 62, 203-206.

Viirre, E., Cadera, W. & Vilis, T. (1988). Monocular adaptation of the saccadic system and vestibulo-ocular reflex. Investigative Ophthatmology and Visual Science, 29, 1339-1347. Zee, D. S. & Levi, L. (1989). Neurological aspects of vergence eye movements. Revue ~euroZogi~ (Paris), 145, 613-620. Acknowledgements-This research was supported by a grant from the National institutes of Health (EYO-1849) (D. S. Zee) and postdoctoral research fellowships from the Fight for Sight Division of the National Society to Prevent Blindness, in tribute to the memory of Dr Hermann M. Burian and his wife, Gladys, and from the Dana Foundation (A. Oohira). The authors thank Saumitra Das, Adrian C. Laskar and Timothy C. Hain for their excellent technical assistance.