SELECTIVE NONCONJUGATE BINOCULAR ADAPTATION OF …faculty.washington.edu/robi/paper/Schor_non... ·...

Yision Rcs. Vol. 30, No. II, pp. 18274844, 1990 0042-6989/90 33.00 + 0.00 Printed in Great Britain Peqamon Press plc

SELECTIVE NONCONJUGATE BINOCULAR ADAPTATION OF VERTICAL SACCADES AND PURSUITS

CLIFTON M. SCHOR, JERRY GLEASON and DOUGLAS HORNER*

University of California, School of Optometry, Berkeley, CA 94720, U.S.A.

(Received 10 August 1989; in revised form 29 January 1990)

Abstract-Hering’s law describes the equal and symmetrical rotation of the two eyes. It is possible to calibrate the binocular yoking of the two eyes in response to disparate size and/or motion of the two ocular images. It is unclear if the ratio of movements by the two eyes is modified by selective adaptation of each versional system (i.e. saccades and pursuits) or if there is an apparent adaptation of Hering’s law that results from a single underlying process. The latter could be accomplished by vergence (prism) adaptation, which could interact with all versional systems. In this investigation, binocularly stimulated saccades and pursuits were adapted separately for 2 hr to unequal vertical target displacements. Three adaptation paradigms were used; each included a 10% binocular gradient disparity. The adapting stimulus for the pursuit system was 0.25 Hz vertical triangular motion of 20 deg, peak to peak. Two saccade adaptation paradigms included one which emphasized correcting vertical disparity during the pulse component of the saccade, the other minimized the influence of disparity prior to, during and immediately after saccades (vergence paradigm). Yoking ratios (YRs) for vertical pursuits and saccades were compared before and after adaptation. The pursuit paradigm produced marked adaptation of the pursuit YRs while it had negligible effect on saccade YRs. The pulse saccade paradigm adapted the saccade YRs twice as much as the pursuit YRs whereas the vergence paradigm resulted in little adaptation of YRs for either saccades or pursuits. Pursuits adapted to the first paradigm in 15-30 min whereas saccades adapted to the second paradigm in IS-2 hr. These results indicate that there is not a single common nonc!onjugate adaptation mechanism for vertical pursuits and saccades. Results of the vergence paradigm demonstrate that feedback during or immediately after eye movements is necessary in order to stimulate the binocular versional adaptation mechanism. Versional adaptation may be considered as a calibration of Hering’s law.

Saccades Pursuits Version Vergence Adaptation Binocular vision

INTRODUCTION

Calibration of Hering’s law

Conjugate movements of the two eyes nor- mally shift gaze in a fronto-parallel plane, whereas disjunctive movements change gaze to different distances or depths in the sagittal plane. Conjugate and disjunctive responses, which have separate control systems (West- heimer & Mitchell, 1956), are both described by Hering’s law of equal and symmetrical eye movements. Hering (1868) noted that when one eye was occluded, the occluded eye still moved conjugately with the fellow nonoccluded eye. He reasoned that there must be a common innervation sent to each eye. It is this pro- posed common innervation and its subsequent modification which is of interest in this paper. We chose to study the ability of the versional

*Current address: Indiana University, School of Optometry, Bloomington, IN 47405, U.S.A.

Eye movements Hering’s law Comitance

systems to modify this common innervation in more peripheral pathways by analyzing Yoking Ratios (YRs) which are defined here as the ratio of right eye rotation to left eye rotation during a versional movement.

The yoked relationship for conjugate eye movements, which is present at birth (Hering, 1868), is maintained during developmental changes, such as increased interpupillary separ- ation and axial length (Larsen, 1971), both of which will require changes of the binocular yoking relationship because they alter horopter curvature (Ogle, 1950). Yoking is also preserved by a spread of comitance when challenged by minor paresis or temporary noncomitancies (Kommerell, Olivier & Theopold, 1976). In some instances, the eyes can be made to move unequally (nonconjugately) to compensate for anisometropic spectacle corrections (Ellerbrock, 1948; Henson & Dharamashi, 1982; Erkelens, Collewijn & Steinman, 1989; Zee & Levi, 1989; Lemij, 1990). These long-term adjustments of

1827

1828 CLIFIDN M. SCHOR et al.

binocular eye movements are evident during either monocular or binocular viewing, which suggests there is an adaptive process that contin- ually calibrates yoking movements of the two eyes. The maintenance of conjugate eye movements in response to physiological and patho- logical changes as well as optical distortions implies that there is a differential change in the innervational pattern to agonist muscle groups. This differential change in innervational is termed nonconjugate adaptation.

Mechanisms underlying plasticity of Hering’s law

Adaptation of Hering’s law has been demonstrated for both fast saccadic movements (Zee & Levi, 1989; Erkelens et al., 1989; Homer, Glea- son & Schor, 1988; Viirre, Cadera & Vilis, 1988; Snow, Hare & Vilis, 1985; Lemij, 1990) and slow pursuit movements (Schor, Gleason & Homer, 1988; Lemij, 1990). It is unclear if these binocular motor adjustments result from selective adaptation of specific types of versional eye movements (saccades and pursuits), or from adaptation of a common binocular vergence process such as vergence (prism) adaptation (Schor, 1983), which could interact with versional eye movements to produce apparent changes in Hering’s law (Breinin, 1955; Ono & Jam, 1981; Miller, Ono & Steinbach, 1980; Kenyon, Ciuffreda & Stark, 1978). If the version-vergence interaction hypothesis is correct, we expect that aftereffects of specific vergence adaptation to spread or to become generalized to both slow and fast versional eye movements. In contrast, if the selective version adaptation hypothesis is correct, we expect a specific vergence adaptation to produce a non- generalized aftereffect that is restricted to the motor system that has been adapted. In the current investigation, we have selectively adapted vertical saccades or vertical pursuits to unequal binocular ocular image motion. Verti- cal, rather than horizontal versional movements were studied because unlike horizontal fusion, vertical vergence is too slow to adequately compensate for unequal binocular stimuli without some form of prediction or adaptation (Kertesz, 1983; Houtman, Roze & Scheper, 1977). In addition, vertical vergence movements are not contaminated by accommodative vergence fluc- tuations, which contributes to their reliable yoking (Collewijn et al., 1988), and finally, phoria adaptation has been shown to be more complete and faster for vertical than horizontal binocular eye movements (Henson & Dharamski, 1982;

Erkelens et al., 1989). Adaptation to either slow or fast movements resulted in a selective aftereffect in which vertical eye movements were unequal during monocular tracking of the adap tation stimulus but not for the unadapted stimulus. This result illustrates that it is possible to selectively adapt slow pursuits to nonconjugate target motion without influencing the yoking of binocular saccades and vice versa.

METHOD!3

Aftereffects produced by selective adaptation of a specific type of eye movement (saccade or pursuit) were compared for slow and fast versional eye movements. In experiments involving selective adaptation, the eyes adapted to nonconjugate target motion of 10% that was pro- dueed by unequal independent rotation of mirror galvanometers before each eye in the SRI visual stabilizer system (Crane & Clark, 1978). Aftereffects were quantified as the change in ratio of movements of the two eyes (YR) from the preadapted state. These nonconjugate aftereffects need to be examined monocularly (i.e. with the vergence loop opened) to eliminate motor fusion responses to binocular disparity during the test period that could either enhance or minimize the underlying nonconjugate yoking of the two eyes.

Eye movements were monitored objectively with the binocular SRI dual Purkinje eye tracker system (Crane & Steele, 1978). The subject’s head position was fixed in the eyetracker with a mouth bite and head rest. The SRI vision stabilizer system was adjusted to correct for spherical components of refractive error and to neutralize heterophoria as tested by the alternate cover test. Because it is possible that vertical YRs may be a function of horizontal vergence angle (e.g. the mechanical advantage of or innervation to each vertical extra-ocular muscle may vary with changing horizontal vergence angle), all measures of the YR were conducted with horizontal fusion in a closed-loop state while vertical vergence was open-loop. This meridional control was achieved by presenting two long vertical stationary lines (25 deg) that were viewed binocularly in the periphery, and a long horizontal and central vertical line, that were viewed monocularly, and provided a moving stimulus for saccades and pursuits (Fig. 1). The two ocular images were of equal size, and adaptation was to their nonconjugate vertical movement.

Calibration of Hering’s law 1829

FIXATION LINES Width:

VeflUne 8.3 Horl Line 3.6

BMXULAR NSloN LINES @4lfh =wl. Width 19’

5.1”

I 3.G b

STIMULUS TARGET

Fig. 1. The monocular tracking stimuius consisted of a high contrast opaque horizontal and vertical line superimposed on a uniformly illuminated background. Subjects were instructed to fixate the intersection of the horizontal and vertical lines throughout the session. In addition, two sets of two parallel, vertical lines were placed iu the right and left eye channels of the SRI visual stabilizers to provide a horizontal binocular fusion lock while the vertical vergencz

loop remained open.

Subjects were instructed to fixate the intersection of the horizontal and vertical line throughout the session.

Prior to each test of saccade or pursuit YRs, voltage analogues of eye position, measured with the SRI eye tracker (Crane & Steele, 1978), were calibrated with a nine-step series of 2.5 deg vertical saccades over a range of 20 deg. Separ- ate third-order polynomials were fit to data obtained from 30 samples (300 msec) at each of the nine stationary monocular left or right eye fixations. These calibration functions were used to transform all subsequent data. Since the current study was concerned with ratios between right and left eye movement, careful calibration was of particular importance because of the sensitivity of ratios to small measurement errors. Test-retest comparisons of successive calibrations were reliable, but only if the subject did not leave the eye tracker between calibrations, For this reason, a calibration was done each time the subject entered the tracker.

The voltage output of the SRI eye tracker is not linear over the range of eye rotations of It 10 deg. There are two main sources for this nonlinear relationship (Crane & Steele, 1978). The first source of nonlinearity is instrument- dependent, small, and associated with large angles of eccentric fixation. The second source of nonlinearity is subject dependent, idiosyncratic, and is due to the irregula~ties of

the optical surfaces in the human eye, To compensate for these nonlinear&s, a best-fit third-order polynomial function was used. A third-order polynomial was chosen to be the calibration function because it has sufhcient power to compensate for the aforementioned nonlinear&& yet larger nonlinearities, caused by subject fixation errors or poor alignment between the subject’s head and eye tracker mouth bite-head rest assembly, could not pass our calibration criteria stated below.

After each eye’s calibration procedure was completed, the results were plotted on a monitor so that each eye position (calibration step) could be compared to the predicted value in both graphical and text format. The calibrations were accepted only if at each of the calibration steps the calculated eye position (using the calibration curve) was within 0.1 deg of the predicted eye position. After the first calibration for a given subject, the eyetracker stage as well as gains and d.c. of mirror galvos in the vision stabilizers were not adjusted for the remaining experiments conducted on a given day. In addition, only one adaptation paradigm was conducted on a given day.

ADAI’TATION PARADIGMS

The following experiments investigated nonconjugate adaptation of vertical versional eye mov~ents to binocular disparity gradients.

Overall afocal magnifier (10%)

Response generalization of the selective adaptation experiments was compared to degree of adaptation of pursuits and saccades stimulated by a 10% afocal overall magnifier (a type of Galilean telescope) {Ogle, 1950) worn before one eye during binocular stimulation for 2.5 hr in an unrestricted environment. 10% was selected on the basis of pilot studies which showed this to be the maxims size difference that could be adapted to in several hours. Subjects wore the afocal magnifier while walking about the building as well as out-of-door. Subjects were encouraged to make frequent vertical saccades, head movements, and visual following responses. As with the other ex~~ments, saccadic and pursuit YRs were quantified before and after the adaptation period.

Pursuit adaptation

This paradigm selectively stimulates unequal binocular vertical pursuit responses for 2.0 hr to

1830 CLIFTON M. SCHOR et al.

nonconjugate vertical triangular motion of the two retinal images. During adaptation, subjects tracked the target represented in Fig. 1 as it moved at 0.25 Hz, 10 deg/sec in triangle wave form, 20 deg peak-peak, that was magnified by 10% before one eye. Saccade-amplitude and pursuit-velocity YRs were compared before and after selectively adapting to this stimulus. This paradigm emphasized adaptation of pursuit movements. However, small amplitude (less than 0.5 deg) “catch up” saccades were common across the adapting field as well as larger amplitude (OS-1 deg) saccades which may occur when the direction of eye movements changed.

Saccade adaptation (pulse paradigm)

Vertical saccades were adapted to nonconjugate (10%) binocular step displacements vary- ing randomly in position to one of nine equally spaced positions in the central 20deg of the visual field. The 20 deg range was selected as a peak amplitude because most naturally occurring saccades rarely exceed I5 deg (Bahill, Adler & Stark, 1975). Step stimuli for saccades ranged in ~plitude from 2.5 to 20deg and each saccade started from random positions at which prior saccades terminated. Eye position at the end of saccades was equally randomized in 2.5 deg steps across the 20 deg field, however small step stimuli were more frequent than large ones (see Table 1). Saccades were stimulated every 500 msec (2 Hz). Shorter intervals were not used because subjects were less likely to attend to the task of foveating the target, and the target was usually repositioned by the time the subject’s saccade was completed. Subjects tracked the nonconjugate stimulus for 2.0 hr, after which the saccadic and pursuit YRs were measured and compared to ratios taken prior to adaptation. This paradigm emphasized correcting the vertical disparity during the pulse component of saccades. However, since typical

Table 1. Probability of occurreuce of saccadic stimuli as a function of step

size

Stimulus Probability amplitude of occurrence

(de& WI

2.5 22.2 5 19.4 7.5 16.7

IO 13.9 12.5 11.1 IS 8.3 17.5 5.6 20 2.8

saccade latency and duration lasted approxi- mately a total of 250-3OOmsec, 200-25Omsec remained for the occurrence of post-saccadic drift, corrective saccades, and disparity vergence. During adaptation, the subjects were allowed to leave the apparatus for short periods while one eye was occluded, however they were encouraged to remain in the apparatus and attend to the tracking task as much as possible. No subjects left the apparatus for more than 5 min of one 2 hr adaptation period.

Open -loop vergence paradigm and fixation disparity

This paradigm de-emphasizes the stimulus for nonconjugate adaptation of the early-pulse component of saccades, post saccadic drift, and corrective saccades, and emphasizes the correc- tion of residual disparity with fusional vergence by presenting the step stimulus to only one eye during the saccade and to both eyes following the saccade. Target position changed randomly as it did in the pulse paradigm only less fre- quently (every 2.7 set or at 0.37 Hz). The stimulus to one eye was blanked from 100 msec before until 6OOmsec after the target was displaced before the fellow eye. 600 msec was chosen in order to insure the completion of monocular corrective saccades prior to binocular stimulation. Then both eyes viewed the stimulus in its new position for an additional 2 sec. During this binocular period, the 10% inequality of target displacement was visible if left uncorrected by the saccadic response. These errors of binocular fixation are sensed close to the fovea and not in the periphery as they were in the pulse paradigm. Accordingly, this paradigm tests if the saccadic system can be nonconjugately adapted in the absence of feedback for binocular versional responses, using only a small post-saccadic vergence stimulus to provide feedback for errors of binocular fixation (fixation disparity). This paradigm minimized the influence of disparity prior to, during, and immediately after versional eye movements.

MKASURRMKNT OF THE YOKING RATIO (PRE AND POST-ADAPTED)

The YR was quantified for both saccades and pursuits before and after each adaptation condition. During evaluation, vertical saccades were stimulated pseudo-randomly every 5 set from the field center to one of 6 positions (up or down, 3, 6 or 9 deg) and then returning to the


center after 1.5 se-c. Movements of both the seeing and occluded eye were sampled at 500 Hz for a I-set period beginning 50 msec prior to the beginning of the pulse stimulus. Saccadic responses were previewed on-line during the ex- periment and were saved for off-line analysis if they met the following five criteria: (1) pre- saccade fixation and difference (vergence) between the two eyes varied less than 10 min arc to insure steady fixation and to preclude ongoing vergence prior to the saccade; (2) there were no blinks or tracking artifacts such as losing the lock on the fourth Purkinje image (i.e. reflection from the posterior surface of the lens); (3) the primary saccades were in the direction of the stimulus; (4) at least 100 msec elapsed between the end of the primary saccade and beginning of additional secondary saccades to allow the vergence phoria to stabilize; and (5) the latency of the saccades was less than 400 msec, to allow sufficient time within the I-set data window to observe changes in phoria following the saccade. Each accepted response was stored as a separate fhe which was analyzed interactively

SACCADE .sTMlLUS ITE FUSE STEP LAE (a)

a ^a d

k r, 29

c- az W8* B

E -1

0 200 400 600 800 1000

off-line. Using these five criteria, depending on the subject between 80-98% of the trials were accepted. A total of 72 saccades were stored for off line analysis. Twelve saccades were stored for each of the six target amplitudes.

Figure 2a illustrates the four eye position components of each saccade that were analyzed off line. These included pre-saccadic, pulse, step, and late components. Five data points were sampled, one every 2 msec, over a lO-msec period, for each of the 4 saccade components, and they were averaged separately. Our com- puter algorithm identified the beginning of the saccade with a velocity criterion greater than 60 deg/sec and duration of 20msec. Pre- saccadic eye position was measured beginning 15 msec before the saccade. The pulse eye position was defined as occurring immediately after the lenticular artifact (exaggerated saccade peak amplitude) associated with monitoring the fourth Purkinje image with SRI dual Purkinje eye trackers. The pulse component was deter- mined by eye and was located 30-45msec after the peak saccade amplitude. The step

PURSUrr

(d)

-1 -10 0 200 400 600 300 1000 0 6 10 20 2s 30

TIME (mrrc) TIME ’ ;mc)

Fig. 2. Simultaneous vertical saccadic movements of the right and kft eyes, stimulated monocularly, and their difference (right - left) (vergencc-lower tine) are shown prior to (a) and following (b) binocular adaptation to the 10% afocal magnifier worn over the kft eye. Part (b) illustrates the post adapted vergence component that is synchronized with the onset of the saccade. Simultaneous vertical pursuit movements of the right and left eyes, stimulated monocularly, and their difference (vergence-ce ntral line) are shown prior to (c) and following (d) binocular adaptation to the 10% afocal magnifier worn over the right eye. Part (d) illustrates the post-adapted vergence component which was evident after only 15 mitt

of adaptation.

1832 chFT73N M. &OR et al.

component was defined as 180 msec after the peak amplitude of the primary saccade or immediately before the first secondary saccade. The late component of the saccade was measured 560 msec after the peak amplitude of the primary saccade in order to compare the vergence phoria with the vergence immediately after the pulse of the primary saccade.

Phorias were computed from absolute measures of eye position at each analysis point. Amplitudes from which YRs were computed, were calculated from change in eye position from the pre-saccadic position to the pulse, step, and late positions of saccades. Phorias (right-left eye position) and YRs (right/left eye amplitude) were then plotted for each saccade component as a function of the six stimulus (saccade amplitude) conditions.

During evaluation, vertical pursuits were stimulated with a 0.25 Hz triangular waveform, 20 deg peak-to-peak, for 30 sec. Movements of both the seeing and occluded eye were sampled at 100 Hz for the 30-set interval. Data files from 5-7 different runs were analyzed separately for upward and downward pursuits. After applying a 3 bin smoothing filter, derivatives were taken from differences between adjacent bins. In order to qualify as pursuits, derivatives from the two eyes had to lie between 5 and 20 deg/sec. Data for eye position and velocity was analyzed about 11 positions from 7.5 deg in the upper and lower field in 1.5 deg steps. Data was included in the analysis if the data from the viewing eye was within 0.5 deg of one of the analysis points. Derivative measures (change in eye position) within 0.5 deg of each field position were aecu- mulated separately for right and left eyes. YRs were calculated for each trial by dividing the accumulated total for each position of the right eye by the accumulated total for the left eye field. Means were calculated across all trials. Similarly, phorias were computed for each of the 11 field positions from the mean difference between position measures (right - left eye) within 0.5 deg of each field position. Pursuit phorias were compiled during smooth eye movements and not in the traditional static mode. Pursuit YRs and phorias were then plotted as a function of field position of the unoc- eluded eye for monocular pursuit responses measured before and after each of the adaptation conditions. Similarly an overall pursuit YR was calculated for all data meeting the velocity criteria without regard for pursuit direction and field position. Figure 11 reflects

the change of overall YR from pre to post adaptation.

The change in YRs for saccades and pursuits, are defined as the difference between post and preadaptation YRs. These differences for both pursuits and saccades are expressed in terms of percent, where:

YR change = [YR (post) - YR (pre)] x 100%

The typical standard error of the difference for YR change was 1% for two subjects and 1.5% for one subject, Data for change of saccade and pursuit YRs was grouped for all subjects and averaged for each selective adaptation paradigm in a histogram analysis.

Nonconjugate adaptation of vertical versional eye movements was revealed by comparing the YR in the pre- and post-adapted states. Test-retest variability of YRs on a given day was less than l-2%, although day to day vari- ation was significant for all subjects, Accord- ingly, differences between adapted and unadapted YR were considered as significant if they exceeded the test-retest variability. The pre-adapted state was used as a baseline reference or control condition. However some pre- caution was exercised in interpreting the adaptation as a “post-pre” adapted difference, We have observed some small idiosyncratic noncomitancies in phorias and versional eye movements that vary with eye position and that are not uniformly present in all classes of versional movements (saccades may be concomi- tant while pursuits are non~omi~nt) in all three subjects that we have studied. Some of these noncomitancies are in a restricted portion of the visual field or in a unique direction in which they are reduced or corrected by the adapting stimulus, while other noncomitancies are exaggerated by the adapting stimulus. In the first case of advantageous adaptation, no change in the pre-adapted state usually occurs. This does not necessarily indicate an inability to adapt, but rather a lack of necessity to adapt. In the second case of disadvantageous adaptation, differences in the pre- and post-adapted states may exceed the magnitude of the adapting stimulus as a result of the contribution of the pre-adapted noncomitancy.

Three subjects, one of whom was an author

(JG), served in each of the adaptation paradigms. Ages ranged from 20 to 35 yr, and all subjects were isometropes whose refractive errors were less than 0.5 D. Each subject under- went each adaptation paradigm twice, once each


with the magnification stimulus before each eye. Results for adapting the left eye to magnification are not shown because they were similar, but opposite in direction to aftereffects of right eye magnification. These equivalent results serve as a control to illustrate that changes in YRs were not caused by fatigue during the 2-hr adaptation period. All graphs are of results from subject (JG) which typify those of the other subjects except where noted. Day to day variations are illustrated by comparing preadap tation results for various adaptation paradigms. These variations were normalized by taking pre- and post-data for a given paradigm on the same day.

RESULTS

Overall afocal magnifier (10%)

Subjects adapted for 2.0 hr to a 10% overall magnifier worn in the spectacle plane before the one eye in order to demonstrate nonconjugate

PURSUIT YOKING RATIOS (R/L)

o.e! - 1 . , . , . , , - 1 -6 Doltlw&Pu&TT: 0 “PWLD P”FLm 9

---8_PREADAPl --B-PREADAPT ~PCSTADAPT ---cposTAcwT

RATIO CHANGES PHORIA CHANGES

binocular adaptation of both saccadic and pursuit eye movements to a simulated anisometropia. Figure 2a, b illustrates vertical saccadic movements of the right and left eye, stimulated during monocular (right eye) viewing, for their difference (R - L) (bottom line) prior to (a) and following (b) adaptation to the 10% afocal magnifier worn over the left eye. Following adaptation, the change in vergence was synchronized with the onset of the saccade. The difference in amplitude of the two saccades is equal to the 10% adapting stimulus worn over the left eye. Figure 2c, d illustrates 30s~ of monocular (right eye) vertical pursuit tracking (20 deg at 0.25 Hz) for the right and occluded left eye, and their difference (R-L) (central line) prior to (c) and following (d) adaptation to the 10% afocal magnifier worn over the left eye. Changes in YRs were clearly evident for both saccades and pursuits.

Figure 3a, b compares the computed pursuit YRs plotted as a function of field position for

PURSUIT PHORIAS (R-L) (W)

1.0

0.5 1 -0.s f

0 3 6

UPWARD PURSUIT:

0.6

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‘.“I -

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Fig. 3. Computed pursuit velocity YRs are plotted (a) for one subject as a function of vertical field position, prior to and after adapting to the 10% afocal magnitkr worn before the right eye. Change in the velocity ratios, resulting from adaptation are plotted in panel (b). Works during pursuits are- plotted in (c) as a function of vertical field position, prior to and after adapting to the same afocal magnifier. Change in vertical phoria, resulting from adaptation is plotted in the lower right resembles the change

in velocity YR curve on the lower left.

1834 CLIFTJN M. !?~HOX et &.

YOKING RATIOS (R/L) PHORIAS (R-L1 tw

o.e5! - 1 . , . , , . I. I _ I.

-12 -9 -6 -3 0 3 6 9

0.85!.. .,.,.,.i.,., -1 -0.254.. -,-1 -,.,.,.,.I -12 -9 -6 -3 0 3 6 9 12 -12 -9 -6 -3 0 3 6 S I2

LEFT EYE POSITION (DEGI LEFT EYE POSITION IDEG)


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oPuLs& aSTEP A LATE

-1.0-r , . * . I . , . I . I 9D 6D 30 3u 6u Su

OPULSE q STEP A LATE - PRE SACCADE PtiORIA

Fig. 4. Saccade YRs for pulse, step and late components arc plotted in the left column for one subject as a function of right eye field position prior to (a) and following (b) adaptation to an afocal magnifier worn before the right eye. Change in YR, resulting from adaptation (c) is plotted below. Saccade phorias measured at the pulse, step and late components of saccades are plotted in the right column for one subject as a function of right eye field position prior to (d) and following (c) adaptation to an afocal magnifier worn before the right eye. Change in phoria, resulting from adaptation is plotted in the lower curve (f). Pre-saccade phorias are shown by the solid line in each plot. The derivative of the change in phoria

resembles the change in saccade YR shown in c and f.

one subject before and after adapting to the 10% magnifier before the right eye. Prior to adaptation, the two eyes had equal pursuit gain (YR = 1) in the upper field. Following adap tation there was a 7.5% increase of the pursuit YRs in the upper visual field. When the same subject adapted to a 10% magnifier before the left eye, the pursuit YRs decreased by as much as 15% below 1.0 in the lower field of gaze. Analysis of the pursuit vergence phoria for the

same adaptation conditions is represented in Fig. 3c, d. Figure 3d illustrates there was an increase of a right hyperphoria in the upper field and left hyperphoria in the lower field that equaled 10% of the stimulated pursuit eye movement. The phoria increased most abruptly in the field where there was the greatest adaptation of the pursuit velocity YR.

Saccadic YRs for the overall magnifier adap tation condition are shown in Fig. 4a, b. Note


PURSUIT YOKING RATIOS (R/L)

RATIO CHANGES

f::;

cc&w UP -0.2 * - . . . . . . s . . _

PURSUIT PHORIAS (R-L)

(fw

PHORIA CHANGES

:r:1’“‘:

Fig. 5. Pursuit phorias and velocity YRs arc analyzed as they were in Fig. 3 in response to the selective pursuit adaptation paradigm in which the image motion was 10% greater for the right than left eye.

the small horizontal misalignment of data points for pulse, step, and late components; this reflects their unequal averaged amplitudes. Sac- cadic YRs for the pulse, step and late components of the saccade changed for all safe amplitudes by approx. 5% when either eye wore the adapting lens. As with pursuits, there was also an adaptation of saccadc phoria that equaled 5% of the saccade amplitude (Fig. 4c, d). The derivative of the phoria function approximated the amplitude of the YR function for saccades. These results provide a clear dem- onstration of changes in the YR for pursuit and saccadic eye movements that occur after only 2 hr of adaptation. The question remains whether there is selective a~p~~on of the YR for specific types of versional eye movements. This question is addressed by comparing the results of the pursuit, pulse, and vergence adaptation paradigms.

Pursuit adaptation

Subjects adapted binocularly in the eyetracker apparatus for 2.0 hr to vertical triangular motion that was 10% greater in the left than

right eye. Figure Sa, b compares the pursuit YRs before and after the pursuit adaptation session. Prior to adaptation, pursuit YRs varied across the field, reaching a peak amplitude at 1.5 deg elevation. The YR reduced in the lower field along with a gradual increase in the left hyperphoria in downgaze. Following adaptation of the right eye to the 10% movement magnification there was a 5-7% increase of the pursuit YR across the visual field (Fig, Sb). Right hyperphoria increased in upgaxe and right hypophoria increased in downgaze (Fig. Jc, d). Following adaptation to the 10% movement magnification before the left eye, there was an 8% reduction in the pursuit YR across the visual field. The phoria also adapted to the pursuit paradigm by increasing left hyperphoria in upgaze and right hyperphoria in downgaze by 5% of the stimulated pursuit movement. Be- cause the baseline velocity ratios and phorias were optically reduced by the adapting stimulus, the amount of adaptation was less than 10%. However, the post-adaptation results illustrate pursuit responses that correct 80% of the adapting stimulus. These changes occurred rapidly for

1836 CLIFION M. SCHOR et d.

YOKING RATIOS tR/Lt PHORIAS (R-L) Meg)

(a) 5 0 0

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LEFT EYE POSlTlON tDEG)

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I A A

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s Y

90 6D 30 3U 6U 9U

OfJusE n!sTEP A LATE - PRE SACCADE PHORIA

Fig. 6. Saccade YRs and phorias are analyzed as they were in Fig. 4 in response to the selective pursuit adaptation paradigm in which the image displacement was 10% greater for the ri& than left eye.

two of the subjects, within IS-30 min of the adapting period, based upon their observations of diplopia, and in an hour for the third subject. In all cases the pursuit adaptation was a more rapid response than observed below with the saccadic adaptation paradigms.

Early components of saccadic YRs (pulse and step) demonstrated little if any change as a result of pursuit adaptation to movement mag nification before either right or left eye (Fig. 6a-c). However, the late component was shifted by several percent in a direction that would minimize the disparity gradient produced during the pursuit adaptation period, The appearance of

graded changes in the post saccadic phoria (Fig. 6d-f) suggests that a nonspecific vergence adaptation could be responsible for some of the pursuit aftereffect. However the change in post saccadic phoria was too smali to account for all of the changes observed in pursuit gain across the visual field. These results demonstrate a selective adaptation of pursuit eye movements, most of which does not become generalized to saccadic eye movements.

Saccade ~ptati~~ (pulse pu~~igrn~

The pulse paradigm emphasized adaptation of saccadic eye movements. Subjects adapted

calibration of Hering’s Iaw 1837

PtJRSUtT YOKING RATIOS tRlL1 PURSUIT PHORIAS (R-L) t+l)

(a) 1.1


-l.O! - , - I . I . I . * .

0 3 6

U~~DP~~

T 1 . , . 1 . 1 . , .

UP

-6 -+--$&&IT

6

~UfWAROPURSUlT

Fig. 7. Pursuit phobias and v&city YRs are analyzed as they were in Fig. 3 in response to the puke-saccadic paradigm for the right eye.

binocularly for 2.0 hr in the eyetracker apparatus to randomized vertical step displacements that were 10% greater in one eye.

During adaptation, several phases were evident. The changes in saccadic YR were first indicated by the subjective disappearance of diplopia after l-l.5 hr of adaptive tracking Compaq to 15-30 min to note changes in diplopia during the pursuit adaptation paradigm. The eyes always adapted to one direction of gaze before the other (up or down). The direction of preferred adaptation resulted from a consistent uniform shift in vertical heterophoria that reduced disparity during adaptation in one field of gaze and increased diplopia in the other field of gaze and sometimes in the central field. For example, subjects JG and MN always had an increase in right hyperphoria within 5 mm when either the right or left eye adapted to mag~fi~tion. This phoria shift demonstrates an early phase of adaptation to gradient disparity which is followed by nonconjugate gain adjustments of the two eyes.

Figure 7a, b compares pursuit YRs measured before and after pulse-saccade adaptation. Prior

to adaptation, pursuit velocity was slightly greater for the left eye (YR = 0.95) across the visual field. Following adaptation to the left eye magnification, there was little if any change in the velocity ratio. Following adaptation to the right eye magnification, there was a 5% increase in the pursuit YR in the central 3 deg of the visual field (Fig. ?a, b). Adaptation to the pulse paradigm resulted in a gradual increase in left hyperphoria in upgaze when the left eye was magnified and right hyperphoria in upgaze when the right eye was magnified (Fig. 7c, d). As with the other adaptation paradigms, the velocity ratio functions could be approximated by the derivative of the phoria functions.

The pulse paradigm resulted in an abrupt change in vergence that was synchronized with the onset of saazades. The saccadic YR decreased by 6% across the field after adapting to left eye magnification, and increased by the same amount after adapting to right eye magnification (Fig. 8a, b). Similarly, saccade phorias changed from right hyperphoria in lower gaze to left hyperphoria in upper gaze following

1838

YOKING RATtOS (R/L)

CLIFTON M. !kHOR Ct 4th

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0 B =

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8 0 El

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1 -1.04 1 . , I . I - I . ,

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Fig. 8. Saccade YRs and phorias are analyzed as they were in Fi&. 4 in response to the selective pulse-mccade adaptation paradigm in which the image di&cunent was 10% greater for the right than

the kR eye.

adaptation to left eye magnification, and they changed from left hyperphoria in lower gaze to right hyperphoria in upper gaze after adapting to right eye magnification (Fig. 8c,d). These phoria changes were approx. 4% of saccadic stimulus amplitude. These results demonstrate a selective adaptation of all three components of saccadic eye movements that only generalized to pursuit eye movements in limited regions of the visual field even though the pursuit system was able to adapt more completely and rapidly than saccades to an appropriate stimulus (Fig. 5).

Open-loop vergence paradigm and fixation &- purity

During the open-loop vergence adaptation paradigm, randomized step stimuli were only visible to one eye. Static targets were viewed binocularly for 2 set, 600 msec after the target was stepped to its new position. Subjects adapted for 2.0 hr in the eyetracker apparatus to randomized amplitudes that were 10% greater in the left or right eye. This was the most difficult paradigm to adapt to and all subjects continued to perceive diplopia at the end of the


PURSUIT YOKING RAmOS (R/L) PURSUtl PHORIAS (R-L) wgi

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Fig. 9. Pursuit phorias and velocity YRs are analyzed as they were in Fig. 3 in response to the open-loop vergence paradigm in which post-saccadic image displacement was 10% greater for the right than left eye.

2-hr adapting period. Figure Qa, b illustrates the YR for pursuits before and after the adaptation. Following the vergence adaptation paradigm in which the right eye was magnified, there was a small increase in the pursuit YRs in the central 3 deg of the visual field. Follow- ing vergence adaptation paradigm to left eye magnification there was a nonuniform decrease in the pursuit YRs of 10% in the lower field of gaze. There was also a progressive increase in left hyperphoria in upgaze following adaptation to left eye magnification, however there was only a modest increase in left hyperphoria in downgaze following adaptation to right eye ma~fi~tion (Fig. Qc, d). The two other subjects demonstrated little if any adaptation of the pursuit YR following either the saccade-pulse or vergence adaptation paradigms.

In sharp contrast to the saccade aftereffects of the pulse paradigm, there were only modest changes in the saccade YRs following adaptation in the vergence paradigm. After adapting to left eye magnification, there was a 4% decrease in the saccade YRs for a11 three

components (pulse, step and late) only in the upper field of gaze, Following adaptation to right eye magnification, there was very little or no change of the saccade-pulse amplitude ratios and phorias (Fig. load). Clearly the vergence paradigm was less effective than the pulse paradigm in adapting saccadic YRs. These results demonstrate that nonconjugate adaptation of saccades does not result from small corrective saccades during the 2-set binocular period, and that it is necessary to have feedback for binocular disparity during or immediately after the version response in order to achieve adaptation of the saccade YR. In the vergence paradigm, disparity feedback was only available from errors of binocular fixation of the static target at the end of its step displacement. These steady state errors of binocular fixation (fixation disparity) were corrected with fusional vergence responses well after the completion of the versional saccade. These corrective movements were sufficient to cause a modest adaptation of the pursuit YR, however the magnitude of the aftereffect was smaller and restricted to a limited region of the visual field in comparison to

1840 CLIFTON M. &XOR et al.

YOKING RATIOS (R/L)

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Fig. 10. Saccadic YRs and phorias are analyzed as they were in Fig. 4 in response to the open-loop vergence paradigm in which post-saccadic image displacement was 10% greater for the right than the

left eye.

aftereffects of the pursuit and afocal magnifier paradigms.

The results of the three selective adaptation paradigms for all three subjects are summarized in the histogram shown in Fig. 11. The histogram represents the average YRs of all field positions for saccades and pursuits. Results for the step component, and to a lesser extent for the late component, of saccades (not shown) were similar to that of the pulse component. Inspection of the figure clearly illustrates that the pursuit adaptation paradigm had a marked effect on pursuit YRs and negligible effect on saccades, and that the pulse-saccade paradigm

altered saccade YRs by more than twice the amount that pursuits were modified. However, the saccadic open-loop vergence paradigm, which attempted to adapt open-loop vergence (phoria) without the benefit of feedback from versional eye movements, was not effective. These results demonstrate that YRs for pursuits and saccades can be altered independently. They indicate that vertical pursuits and saccades do not share a single common adaptation mechanism and that calibration of Hering’s law can not be explained solely by vergence (prism) adaptation. Results of the vergence adaptation paradigm demonstrate that feedback during


YOKING RATIO CHANGE AVERAOW own ALL StQeCm

&WY

2

7.owi

Sam

!I z

5 %ca%

5 zfm%

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Fig. 11. The histogram provides a summary of results of all three selective adaptation paradigms, averaged for all three subjects. Average YRs of all field positions for pulse saccade amplitude and pursuit velocity are shown for each adap tation paradigm. Pursuit adaptation had a marked effect on pursuit YRs and negligible effect on saccades, and the pulse-saccade paradigm altered saccade YRs by more than twice the amount than pursuits were modified. However, the saccade open-loop vergence paradigm, which attempted to adapt open-loop vergence (phoria) without the benefit of feedback during or immediately after versional eye movements, was not effective for changing YRs of either saccades

or pursuits.

or immediately after eye movements is necessary to calibrate the YR described by Hering’s law.

DISCUSSION

Selective adaptation of yoked versional eye movements

Comparison of results from the three selective adaptation paradigms suggests that there is some independent nonconjugate binocular adaptation of the various slow and fast versional control systems. Pursuits may adapt nonconjugately while saccades do not and vice versa. There is also a minor degree of generalized aftereffects in which nonconjugate binocular pursuit adaptation also produces small inequal- ities of conjugate saccades during monocular tracking. This small generalized aftereffect may result from position corrective saccades which occur during the binocular pursuit adaptation paradigm. Indeed, the degree of generalization was greatest in the subject who had higher amplitude and greater preponderance of “catch up” saccades during the pursuit adaptation period than found for other subjects. We observed more cross-adaptation from saccade adaptation to pursuits than from pursuit adaptation to saccades (Fig. 11). With our 2-hr adaptation period, there may have been some adaptation of a process that is separate from pursuits and saccades, that subsequently

interacted more with continuous pursuits than the pulse component of s&ades. Fusional vergence is a possible candidate for the separate system because its continuous control could interact more with smooth pursuits than saccades.

Both the saccadic pulse and pursuit adap tation paradigms provided some opportunity for vergence (prism) adaptation. The SOOmsec step stimulus for saccades could stimulate vergence after the completion of the saccade. As mentioned in the methods, typical saccade latency and durations were 2X&300 msec, which left an additional 200-250msec of the step to stimulate adaptation of vergence. During the pursuit adaptation paradigm, the binocular disparity changed continuously and may have also provided an opportunity for adjustments of positional phorias across the visual field. How- ever, the role of vergence adaptation is dimin- ished by the results of the vergence adaptation paradigm. It resulted in smaller pursuit aftereffects than did the other paradigms for two of the three subjects, even though the average pursuit aftereffect of the three subjects shown in Fig. 11 was the same (2.6%) as the pursuit aftereffect resulting from the pulse-saccade adaptation paradigm. Taken together, these results demonstrate selective nonconjugate binocular adaptation of saccades and pursuits as well as the possible adaptation of a separate interactive system such as vergence.

The high degree of selectivity of aftereffects indicates that changes in the YR do not result exclusively from an interaction of all versional eye movements with a single mechanism, but rather independent mechanisms for each versional system appear to underlay the continued calibration of Hering’s law. In addition, as demonstrated by the vergence paradigm, feedback during or immediately after eye movements is necessary to calibrate Hering’s law. It is possible that the highly selective aftereffects were specific to the conditions of adaptation (i.e. frequency, amplitude and velocity of the tracking stimulus). We are currently conducting experiments to test how generalized the aftereffects of pursuit adaptation are across these stimulus parameters.

Hering’s law; innateness and plasticity

Hering’s law of equal innervation states that corresponding muscles of the two eyes are always equally innervated. While Hering (1868) stressed that the coordinated movements of the

1842 CLIFTON M. SCHOR etal.

eyes resulted from an innate organization of common controllers or motor drives for the two eyes, he states that there exists a certain ability to accommodate these “unchangeable” prin- ciples in response to changed relationships (p. 23). The term unchangeable reflects the concept of innateness. Although he did not elaborate upon this ability to modify the control properties of ocular motility, nor did he apply this concept to his laws, it may be inferred that Hering was aware of some degree of tuning of oculomotor control that would maintain the precise yoking of the two eyes. Hering observed the innateness of yoked movements in newborn children, he was aware of growth and develop mental changes of the eyes, as well as the effects of trauma and peripheral lesions on the extra ocular muscles, and the demands these events placed upon maintenance of yoked versional eye movements. However, he lacked the technology to allow him to observe and substantiate the subtle degree of tuning or ongoing calibration of the YR that has recently been observed in response to physiological and environmental demands (Viirre, Cadera & Vilis, 1987; Schor et al., 1988). Indeed, these changes are so subtle that they approximate the resolution limits of current technology for quantifying movements of the eye.

Physiological correlation of the yoking calibration process

The calibration of the YR, by itself, does not constitute a violation or invalidation of Hering’s law. Indeed, there is considerable evidence for the existence of common motor drivers or controllers of muscle groups of the two eyes (Nakayama, 1975). However, peripheral to these common sources of innervation, there are independent saccadic pulse generators (Sparks, Gurski, Mays & Hickey, 1986). It is possible that calibration occurs at this peripheral stage of neural control. For example, if firing duration of selective groups of burst neurones were calibrated to control amplitude of saccades (Abel, Schmidt, Dell’Osso & Daroff, 1978) this could account for the selective adaptation of yoked eye movements that have been implied for restricted portions of the motor field (Henson & Dharamski, 1982). These burst cells stimulate individual motoneurones whose firing rate in- creases monotonically over limited ranges of orbital eye position (Keller & Robinson, 1972). It is also possible that independent motor maps for the two eyes at higher levels such as in the

occipital cortex, frontal eye fields, and superior colliculus could be reprogrammed to accom- plish nonconjugate adaptation of the two eyes in specific directions of gaze (Henson & Dharam- ski, 1982). An adjustment of perceptual maps of visual space as a result of oculomotor adaptation has been demonstrated by Moidell and Bedell (1988) who produced a spatial distortion in the form of a monocular partition error (Kundt asymmetry) (Ogle, 1950) that resulted from calibration of monocular saccades using the electo-optical parametric adjustment paradigm of McLaughlin (1976) in which retinal image feedback is altered during a saccade. These perceptual changes persisted during steady fixation in the absence of saccades and amounted to 38% of the motor adaptation stimulus (0.8 deg of 2.1 deg stimulus). A remapping of striate cortex (somatosensory Sl and Sll) in monkey has been demonstrated for fovea1 representation after ablation of foveas using laser coagulation (Heinen & Sakavenski, 1988). However, the reorganization of the recep- tive fields in the prior fovea1 representation occurred 75 days after the lesion which is a much longer time span that observed in the behavioral remapping study by Moidel and Bedell (1988).

Reprogramming could easily be accomplished for cells which encode absolute (head reference) direction in space. These cells com- bine eye position information with retinotopic target position (Sakata, Shibutani & Kawano, 1980). Amplitude of saccades directed to specific orbital positions could be changed by altering information about eye position. The cerebellum is another possible supranuclear site for adaptive regulation of saccades. Experimental lesions of the dorsal vermis in trained monkey prevents monocular adaptation of the pulse component of saccades (Optican & Robinson, 1980) while lesions of the flocculus prevents monocular adaptation of the step component of saccades to match pulse height (Zee, Yamazaki, Butler & Guger, 1981). The main difficulty with these supranuclear explanations is that adaptation would be expected to influence the two eyes equally. However, Vilis, Snow and Hare (1983) demonstrated that reversible cerebellar lesions induced by cooling resulted in binocular saccades of unequal amplitude. Separate control of the two eyes first appears at the PPRF (paramedian pontine reticular formation) where burst neurones project directly to ipsilateral motoneurones and to the contralateral agonist

Calibration of Hcring’s law 1843

motoneurones via internuclear neurones which project up the contralateral medial longitudinal fasciculus. Burst neurones in the rostra1 mesencephalic reticular formation have been shown to control vertical saccadic eye movements (Buttner, Buttner-Ennever 8z Henn, 1977; King & Fuchs, 1979) independently for the two eyes (Gamlin, Gnadt & Mays, 1989). Recently Sparks et al. (1986) have observed some brain- stem neurones in the PPRF of monkeys raised with monocular deprivation that have firing rates proportional to the position of the de- prived eye while other cells have discharge frequencies related to the position of the nonde- prived eye. These neurones provide independent left and right command signals for the two eyes and could play a role in the calibration of Hering’s law of equal innervation. Independent control of eye movements could result from a loss of internuclear neurones in the MLF or it could be a manifestation of the independent control mechanisms of eye movements seen in reptiles and birds. This interpretation suggests that coordinated, but independent mechanisms control the orbital position of each eye. If there is independent adaptation of gain control of the two eyes it appears easier to reduce monocular gain of one eye than to increase gain of the other (Deubel, Wolf & Hauske, 1982). The difficulty of having adaptation occur in the brain stem is that there is no spatial or orbitotopic mapping or representation to explain the spatially local- ized changes in heterophoria observed by Hen- son and Dharamski (1982). Possibly, there are two or more adaptive processes, where spatially specific adaptation is due to vergence adaptation controlled in a supranuclear spatial map, and general, nonspatially-selective adaptation of yoked version eye movements that is due to modification within the brain stem.

The results of this study and others (Henson & Dharamski, 1982; Erkelens et al., 1989; Zee & Levi, 1989; Viirre et al., 1988; Lemij, 1990) indicate that the motor responses of the two eyes adapt independently to unequal retinal image size, motion, and feedback. This nonconjugate binocular adaptation is only achieved if the two eyes are adapted simultaneously to unequal ocular image motion or displacement. If the oculomotor system is adapted monocularly to altered feedback caused for example by tenectomy, both the stimulated and occluded eye exhibit the same motor aftereffect (i.e. conjugate altered gain for saccades) (Snow et al., 1985). Clearly nonconjugate adaptation to

binocular disparate stimuli is a response driven by binocular sensory-motor fusion.

Acknowledgemenr-This work was supported by NE1 grant no. EYO 3532-09 to CS.

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