- Email: [email protected]
“Passive suppression” of optokinesis by stabilized targets
scion Res. Vol. 28, No. Printed in Great Britain
9, pp. 10234029, 1988
“PASSIVE
0042~6989/88 83.00+ 0.00 Pergamon Press plc
SUPPRESSION” BY STABILIZED
OF OPTOKINESIS TARGETS
HARRY J. WYATT, JORDAN POLA and MARCIE LUSTGARTEN ~hnu~acher
Institute for Vision Research, State University of New York, State College of Optometry, 100 East 24th Street, New York, NY 10010, U.S.A. (Received 20 July 1987; in revisedform
7 January 1988)
Ahstrati-Subjects gazed passively at a sinusoidally oscillating optokinetic stimulus. They made no attempt to look at a target which appeared, stabilized on the retina at one of several locations, yet the appearance of the target caused rapid and prolonged suppression of optokinesis. Suppression declined (optokinesis increased) as target eccentricity increased, but could be observed for eccentricities up to 15-2Odeg. We propose that a target moving relative to a background is a stimulus for suppression of optokinesis, depending substantially on the visual properties of the target and not the act of attending to it. Optokinesis
OKN
Suppression
Fixation
Visual stimuli
INTRODUCTION
Optokinetic eye movements are an oculomotor response to movement of a large portion of the visual world; they approximately stabilize the eyes in space (ter Braak, 1936; Jung, 1977; Jung and Kornhuber, 1964; Carpenter, 1977; Robinson, 1981). Since animals with foveas often fixate targets in motion relative to the rest of the world, it is often necessary to prevent optokinesis. We showed earlier that a small target, stabilized on a subject’s fovea, can suppress optokinesis when the subject looks at the target (Wyatt and Pola, 1984). That work did not separate the act of attending to the target (which might in some way “shut off” optokinesis) from the simple visual presence of the target. In the present work, we examined the effect of targets (together with an optokinetic stimulus) presented to subjects who made no e&rt to look at them: even when presented at considerable eccentricity from the fovea, such targets caused suppression of optokinesis. These results were presented in preliminary form at the 1984 Annual Meeting of the Association for Research in Vision and Ophthalmology in Sarasota, Fla.
METHODS
Many of our methods have already been described in detail; here, we emphasize new methods (For further details, see Wyatt and Pola, 1984 and 1987.)
A target (1.5 deg dia.; 0.5 cd/m*) was projected on a rear-projection screen via a high-speed shutter and servomotor-controlled mirror. The target was stabilized on the retina with respect to horizontal eye movements. The optokinetic stimulus field was created with a “planetarium” type projector: holes were drilled in a small drum in quasi-random arrangement; a compact filament-sours at the center of the drum produced pinhole images of the filament on the walls, ceiling, and floor. A typical image had dia. 2 deg and luminance 0.01 cd/m*; average spot density was approx. 1 spot/42 deg’ (average area per spot was a square 6.5 deg on a side). The drum was rotated by a servomotor (Electrocraft), producing horizontal sinusoidal field motion, 30deg peak-topeak at 0.5 Hz. The field motion was made open-loop by adding a signal of eye velocity to the sinusoidal signal frhe motor/drum combination could not fully stabilize the field for saccadic eye movements or fast phases of OKN; drum excursion was about 5&60% of saccade length. We have obtained similar results using closed-loop motion of the field (unpublished results)]. The advantage of the open-loop field is that, during smooth movements of the eye, the average retinal behavior of the field was known. Sinusoidal field motion continued whether or not the target was present. znst~ctio~~ to &jects
1023
Subjects were instructed to remain “passive”
1024
HARRY J.
WYATT
throughout each trial: they were not to attempt to fixate the target or any part of the optokinetic stimulus, but were to gaze ahead; however, they were not to fight any involuntary eye movement that they became aware of. They were to keep their attention at the plane of the wall in front of them, and not gaze into some imagined distance or at an imaginary target. Finally, they were asked to keep their gaze roughly horizontal, which was achieved with little effort (Wyatt and Pola, 1984). Experimental protocol and ~ali~rati5~s
Subjects were dark-adapted for about 10 min before a session. The eye position signal was calibrated and target stabilization checked before and after each trial. At the start of a trial, the target disappeared and oscillation of the field began, After 3-5 cycles of field oscillation, the experimenter initiated the suppression portion of the trial. At the beginning of the next cycle of field motion (max velocity left), the target reappeared at a retinal location randomly selected from a programmed set. The trial continued, the subject remaining passive, for approx. 20 more cycles of field motion. On
PI d.
occasional trials, the pre-target portion of the trial was extended for an additional 20 cycles to obtain more data on the passive optokinetic response. Data recording and ana~~si.~
Eye position (left eye viewing monocularly) was monitored with an infrared system. Stimulus field velocity, and horizontal eye position and velocity were recorded on a polygraph. From 4 set before to 4 set after target appearance, eye vetocity was recorded on disk at 125 samples/set. Steady-state responses (with or without the target present) were analyzed by hand to obtain amplitude and phase lag of smooth eye movements with respect to field velocity. Eye velocity near target onset was studied by removing saccades from the data on disk, and averaging together the eye velocity records (aligned at target appearance) for each subject for each experimental condition. Latency of onset of suppression was estimated by comparing eye velocity following target appearance with eye velocity during the pretarget cycle [An example of onset estimation is shown in Fig. 1 (inset)].
7.5”R
30*/
5
15’
R
C
Fig. I. sample eye velocity records from one subject for three locations of target appearance. The bottom trace shows field velocity (&); other traces show eye velocity (da). At the vertical line marked by an arrow, the target appeared at the location indicated at the right of the record. Saccades have been truncated. Inset: segment of averaged records (saccades removed) for the same subject for the target presented 15 deg right. Solid line shows peristimulus segment; dotted line shows averaged data from the cycle preceding the stimulus. Time scale expanded 3 x relative to remainder of figure; time calibration: 100 msec; open triangle shows estimated onset of suppression.
Passive suppression
Subjects
The subjects consisted of six males and females, aged 2045, emmetropic to 5D myopic, uncorrected. Three of the subjects were naive.
RESULTS
Optokinesis
Optokinetic responses to oscillating fields have been described (Wyatt and Pola, 1984). All six subjects showed vigorous optokinesis, with average velocity amplitude of smooth eye movements 28.7 (SD = 13.3) deg/sec and phase lag 42.9 (SD = 11.4) deg relative to field velocity. (Average gain = 0.61.) Onset of suppression
Figure 1 shows sample eye velocity records from one subject. At the time indicated by the arrow, the target appeared. (Eccentricity indicated at the right of each trace.) It is apparent that suppression appeared rapidly and that it was substantial, even when the target was not on the fovea. The inset shows an example of estimation of latency of onset on an expanded time scale. We performed experiments on five subjects with the target appearing randomly at one of a set of the following locations: fovea1 and 7.5 and 15 deg left, right, up, or down from the fovea. The latencies for onset of suppression were estimated as described in Methods. Since latency was not found to vary systematically with meridian, the results were pooled for each eccentricity. The latencies in msec were: target appearance at the fovea, 150 f 30 SD (range 104-184); at 7.5 deg eccentricity, 186 f 35 (range 120-248); and at 15 deg eccentricity, 246 + 59 (range 168-384). The results in this paper are for targets appearing when the field was moving with maximum velocity leftwards. Pilot experiments showed no systematic difference between this condition and that with maximum velocity rightwards. If the target appeared when the field was at maximum excursion left or right (velocity zero), temporal features of the onset of suppression were difficult to observe [Smooth eye velocity was then low at the moment of target appearance. Also, relative target/field motion at the moment of appearance was zero, and relative motion may be responsible for suppression (see Discussion)].
Suppression in the vector representation
1025
steady
state-d#erence
The inset in Fig. 2 is a diagram showing how steady-state suppression is plotted. The notation used is based on the “difference vector,” which represents the d@rence that the presence of the target makes in the optokinetic response (Wyatt and Pola, 1984). For purposes of graphic representation, we plot minus one times the difference vector (“-D” in the inset). The basic points to be noted about this representation are that: (i) a smaller vector indicates less suppression; and (ii) a vector that points straight up to 1.0 (i.e. -D being the same as F) indicates perfect suppression (a stationary eye). The remainder of Fig. 2 shows data for three subjects. The target appeared at the fovea, or 7.5 or 15 deg away from it horizontally or vertically (The location 15 deg left was displaced upwards 3 deg to move the target out of the blind spot.) The figure shows that suppression was maximal at the fovea and substantial over a considerable region; however, it decreased as the target moved to more eccentric locations. This fall-off was especially rapid along the vertical meridian for two out of the three subjects shown (We observed this asymmetry for three out of five subjects). We performed further similar experiments using a set of target locations consisting of the fovea and 11 and 22 deg left and right. The two subjects tested still showed considerable suppression for 22 deg target eccentricity [At 22 deg, the lengths of the vectors describing suppression-see Fig. 2-were 0.35 (left) and 0.61 (right) for one subject and 0.71 (left) and 0.66 (right) for the other]. The results described so far were obtained with a target that was considerably brighter than the elements of the optokinetic field (see Methods). To examine the effect of relative target luminance on suppression, we reduced target luminance to match the field elements and ran further experiments of the same type as shown in Fig. 2. With the dimmer target, the latency for suppression became longer and quite variable, and onset was often difficult to pinpoint; however, once suppression developed, the suppression was again found to be considerable and sustained for two subjects tested. Compared to the brighter target, the length of the vector representing suppression (see Fig. 2) was reduced by 0.27 for one subject and by 0.04 for the other (averaged over target positions). Similar
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HARRY J. WYATT et al.
F
Ldl
Right
I+-- 7.5’--+
Down
Down
Fig. 2. Inset: Diagram of vector notation used to indicate suppression in the steady state. At the left of the inset are the passive optokinetic (F) and suppressed (T + F) responses: length of each vector represents the velocity amplitude of the smooth eye movement (deg/sec), and the angle between the vertical axis and each vector represents the phase lag of eye velocity with respect to field velocity. At the right, the (normalized) difference vector “D” is derived: the passive optokinetic response. (F) is taken as the reference; i.e. its phase lag is set to zero and its amplitude to unity. The suppressed response (T + F) is now scaled in amplitude relative to F, and its phase lag is shown relative to F. The difference vector is then defined as the vector value of F minus T + F, it represents the da@krence that the presence of the target makes in the optokinetic response (Wyatt and Pola, 1984). Finally, for purposes of graphic representation, minus one times the difference vector (,‘-D” in the inset) will be plotted. Note that if -D equals zero, there is no suppression (T + F is identical to F); if-D points straight up to I.0 (is the same as normalized F), suppression is perfect since T + F is zero. This notation also contains phase information: if the vector lies counter-clockwise from upwards, the phase lag of the suppressed response (T + F) was between 0 and 180 deg greater than the phase lag of the passive optokinetic response (F). Clockwise from upwards indicates a phase lag of T + F less than F (or more than 180 deg greater than F). The remainder of the figure uses the vector notation to plot suppression for 3 subjects for various target locations in the steady state. Retinal target location is indicated by the base of each vector.
results were obtained when the luminance of the field components was increased (instead of target luminance decreased) by substituting a tungsten-halogen source for the standard source.
Eflects of attending to a given target location on suppression onset We hypothesize in the Discussion that a substantial amount of suppression occurs without attending to the target; however, it is possi-
Passive
ble that appearance of a target causes a subject to attend to the new target, even without deliberate effort to do so. Such attention could be involved as an intermediate step in producing suppression. To begin examining this possibility, we performed an additional experiment: the same field was used as before and the (brighter) target appeared at 7.5 deg left or right of the fovea. Subjects were told to attend to the right-hand location and push a button when the target appeared there, but to ignore the target (which they were told was “only for a control”) when it appeared at the left-hand location (20% of the time), Onset of suppression was examined for each of the two locations. Figure 3 shows computer-averaged smooth eye velocity data for two subjects: the solid curves are for target appearance at the attended location and the broken curves are for appearance at the “ignored” location. There was no obvious difference in onset of suppression for the two locations; i.e. the task given the subject made no apparent difference in the onset of suppression. DISCUSSION
The results described here indicate that the presence of a target, in relative motion to a stimulus field, suppresses the optokinesis that the field by itself would elicit, even when subjects do not pay attention to the target. It is known from everyday experience that looking at a target suppresses optokinesis to some degree, but previous work differs in assessing the degree. For the case of pursuit against a background, some work has shown a reduction of gain, suggesting incomplete suppression
suppression
1027
~Collewijn and Tamminga, 1984; Yee ef al., 1984; Barnes and Crombie, 1985); other work has shown a reduction of gain during pursuit initiation, but little or no reduction at later times (Keller and Khan, 1986); some work has suggested an enhancemenl of pursuit against a background (ter Braak, 1957, 1962; Hood, 1975). We have reported that with experienced subjects, steady-state pursuit of an open-loop target against a background shows very little effect of the background (Pola et al., 1983). Using an optokinetic stimulus field and stationary edges, Murasugi et aZ. (1986) observed suppression when subjects attended to the edges, but much less suppression (more OKN) when they attended to the field. In the present work, subjects remained passive; we asked them to continue the same neutral attentional state they were asked to maintain for passive optokinetic responses. We hoped that this would enable us to begin to separate visual from attentional contributions to suppression.
The extent of the spatial domain we observed for passive suppression was impressive: while there was variation between subjects, considerable suppression was observed for eccentricities up to 15 and even 22 deg. In related experiments, Barnes and Crombie (1985) and Murasugi er ai. (1986) found a somewhat more restricted domain: unidirectional OKN was approx. 50% reduced in slow phase velocity when (fixated or attended) targets or edges were 5 deg eccentric. We also found that three out of five subjects showed a horizontally-elongated
1
30’19
1
30*/s
Fig. 3. Experiment to examine effect on suppression onset, of attending to target location. Average smooth eye velocity records arc shown for two subjects. Target onset at the vertical line. Solid lines show responses when target appeared at pre-attended location (7.5 deg R) and subjects responded with a button-pm~; broken lines when target appeared at “ignored” location (7.5 deg L). See text.
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HARRYJ. Wu~rr et al.
suppressive region. This is intriguing, since the sensitive domain for eliciting optokinesis in rabbits is horizontally-elongated (Dubois and Collewijn, 1979a) which may correspond to the rabbit visual streak (Hughes, 1971) and there is evidence suggesting some elongation of a visual streak even in primates which have predominantly centralized retinas (Stone and Johnston, 1981). In addition to an extensive spatial domain, the speed of onset of passive suppression was considerable: for targets 7.5 deg eccentric and less, the average latency was under 200 msec. Furthermore, the suppression was long-lasting, continuing as long as our trials ran. The increases in latency observed for greater target eccentricities may reflect reduced sensitivity of the mechanism detecting the target (see below).* Relative motion-a
stimulus for suppression?
Our results suggest that, provided with an appropriate stimulus, optokinesis begins to be suppressed quite rapidly, without deliberate effort on the part of the subject. The targets presented here were distinguished from the optokinetic field mainly by being in motion *A possible consideration in these experiments is that the target, by directly obscuring a portion of the field, might create part of the suppression by removing part of the optokinetic stimulation. This is unlikely to be a significant effect for eccentric targets, since a 1.5 deg target at 7.5 deg eccentricity occupies only 2.5% of the visual field between 6.75 and 8.25 deg eccentricity and only 0.8% of the visual field at eccentricities less than 8.25 deg. However, targets at the fovea, while covering only a very small part of the visual field, do cover some of the most sensitive part of the retina for optokinesis (Koerner and Schiller, 1972; Dubois and Collewijn, 1979b; Barnes and Hill, 1984; Pola and Wyatt, 1985). We have carried out some experiments using a foveally-centered target consisting of annuli (either o.d. 1.5deg, i.d. 1.0 deg or o.d. 4.0 deg. i.d. 3.0 deg). Such targets caused approximately the same suppression as the standard 1.5 deg target. which was also approximately the same as the suppression caused by a 4.0 deg dia. disk. We interpret this to mean that a contribution to suppression due to occlusion of the field in our experiments is likely to be minor. tThe one exception was a subject who showed small movements approximately opposite to the field while remaining passive; this subject made vigorous movements opposite to the field when looking at the same target. Thus, the general rule was that the eye movements of a passive subject with a fovea1 target were more like optokinesis-i.e. with the field-than the eye movements of the same subject when looking at the target. The same subject showed movements with the field when passive with an extrafoveal target.
relative to the field (They were also usually brighter than the elements of the field, but a bright target would still act as part of the optokinetic stimulus if it moved together with the field). In a natural visual scene, a target in motion relative to a background is often an object of interest, and its seems reasonable to propose that such a target acts as a “stimulus for suppression” of optokinesis. A mechanism of this type could usefully begin preparation for fixation of the target even before a conscious decision to do so, if the mechanism were fast enough and operated over an adequate spatial domain (which the present results suggest is the case). Visual neurons have been observed with receptive fields which are sensitive to targets in motion relative to a background (reviewed in Allman et al., 1985); similar neurons might provide a substrate for the type of effects described here. When our target was similar in luminance to the field components, the rapidity and strength of suppression was reduced (see Results). As noted above, other work with somewhat similar paradigms found more restricted domains of effectiveness for suppression of optokinesis than we have observed. Assuming that some mechanism must detect the target (or edge) moving relative to the field, then that mechanism might reasonably be expected to detect the relative motion more easily when the target is also distinguished by such attributes as luminance, size, color, etc. [e.g. for targets distinguishable from a background only by motion, peripheral targets must be larger than central ones for detection to occur at the same velocity (Regan and Beverely, 19841. Other factors that may contribute to the extensive domain for suppression observed here are: (i) the fairly low density of texture in our stimulus field; and (ii) the 0.5 Hz optokinetic stimulus we used instead of unidirectional stimuli. Relation of passive suppression to attention
be made clear that there is a the passive suppression described here and suppression while looking at a stabilized target. Subjects actively looking at a foveally-stabilized target against an optokinetic field often move their eyes opposite to the field (Wyatt and Pola, 1984; Pola et al., 1983; Lustgarten et al., 1987); however, subjects who are passive in the same stimulus situation generally show some movement along with the fie1d.t It
should
difference
between
Passive suppression
We did not observe a difference in onset of suppression when we asked subjects to attend to one of two locations of target appearance (Fig. 3). In experiments measuring manual responses to similar target appearances, appropriate cueing of the impending target location can shorten subjects’ manual response times (Posner, 1980); however, whether such findings extend to eye movements is not clear (Klein, 1979). If, as suggested above, passive suppression operates via visual structures sensitive to relative motion, it is possible that it might operate (or operate partly) preattentively, cooperating in setting the stage for the attention/ fixation response.
Acknowledgements-Supported by NSF BNS-8519267. We thank John Orzuchowski for help with the electronics and Wayne Grofik for preparation of illustrations.
REFERENCES Allman J., Miezin F. and McGuiness E. (1985) Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. A. Rev. Neurosci. 8, 407430. Barnes G. R. and Crombie J. W. (1985) The interaction of conflicting retinal motion stimuli in oculomotor control. Expi Brain Res. 59, 548-558.
Barnes G. R. and Hill T. (1984) The influence of display characteristics on active pursuit and passively induced eye movements. Expl Brain Res. 56, 438447. Braak J. W. G. ter (1936) Untersuchungen uber optokinetischen Nystagmus. Arch. Neerb. Physiol. 21, 309-376.
Braak J. W. G. ter (1957) Ambivalent optokinetic stimulation. Folia Psychiat. Neurol. Neerl. 60, 131-135. Braak J. W. G. ter (1962) Optokinetic control of eye movements in particular optokinetic nystagmus. Proc. 22nd Int. Congr. physioi. Sci. Leiden, 502-505.
Carpenter R. H. S. (1977) Movements of the Eyes. Pion, London. Collewijn H. and Tamminga E. P. (1984) Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J. Physioi., Land. 351, 217-250.
Dubois M. F. W. and Collewijn H. (1979a) The optokinetic reactions of the rabbit: relations to the visual streak. Vision Res. 19, 9-l 7.
Dubois M. F. W. and Collewijn H. (1979b) Optokinetic reactions in man elicited by localized retinal motion stimuli. Vision Res. 19, 110~1115. Hood J. D. (1975) Observations upon the role of the
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peripheral retina in the execution of eye movements. J. Oto-rhino-lar. Borderlands 37, 1701-1712. Hughes A. (1971) Topographical relationships between the anatomy and physiology of the rabbit visual system. Documenta ophth. (Den Haag) 30, 33-159.
Jung R. (1977) Introduction: an appreciation of early work on gaze control in man and of visuo-vestibular research before 1940. In Control of Gaze by Brain Stem Neurons (Edited by Baker R. and Berthoz A.). Elsevier/North Holland, Amsterdam. Jung R. and Komhuber H. H. (1964) Results of electronystagmography in man: the value of optokinetic, vestibular, and spontaneous nystagmus for neurologic diagnosis and research. In The Oculomotor System (Edited by Bender M. B.). Harper & Row, New York. Keller E. L. and Khan N. S. (1986) Smooth-Pursuit initiation in the presence of a textured background in monkey. Vision Res. 26, 943-955. Klein R. (1979) Does oculomotor readiness mediate cognitive control of visual attention? In Atrention and Performance VIII (Edited by Nickerson R. S.). Erlbaum, Hillsdale, NJ. Koemer F. and Schiller P. H. (1972) The optokinetic response under open and closed loop conditions in the monkey. Expl Brain Res. 14, 318-330. Lustgarten M., Pola J. and Wyatt H. J. (1987) “Hypersuppression” of optokinesis: variation with frequency. Invest, Ophthal. visual Sci. (Suppl.) 28, 314.
Murasugi C. M., Howard I. P. and Ohmi M. (1986) Optokinetic nystagmus: the effects of stationary edges, alone and in combination with central occlusion. Vision Res. 26, 1155-l 162.
Pola J. and Wyatt H. J. (1985) Active and passive smooth eye movements: effects of stimulus size and location. Vision Res. 25, 1063-1076.
Pola J., Wyatt H. J. and Zupnick Y. (1983) Suppression of OKN during visual fixation and pursuit. Invesr. Ophthai. visual Sci. (Suppl.) 24, 27 1. Posner M. I. (1980) Orienting of attention. Q. JI exp. Psychol. 32, 3-25.
Regan D. and Beverley K. I. (1984) Figure-ground segregation by motion contrast and by luminance contrast. J. opt. Sot. Am. A 1, 43342.
Robinson D. A. (1981) Control of eye movements. In Handbook of Physiology Section 1, Vol. II, Part 2 (Edited by Brookhart J. M., Mountcastle V. B., Brooks V. B. and Geiger S. R.), pp. 1275-1320. Am. Physiol. Sot., Bethesda. Stone J. and Johnston E. (1981) The topography of primate retina: a study of the human, bushbaby, and New- and Old-World monkeys. J. camp. Neurol. 196, 205-223. Wyatt H. J. and Pola J. (1984) A mechanism for suppression of optokinesis. Vision Res. 24, 1931-1945. Wyatt H. J. and Pola J. (1987) Smooth eye movements with step-ramp stimuli: the influence of attention and stimulus extent. Vision Res. 27, 1565-1580. Yee R. D., Daniels S. A., Jones 0. W., Baloh R. W. and Honrubia V. (1984) Effects of an optokinetic background on pursuit eye movements. Invest. Opthal. uisual Sci. 24, 1115-1122.
9, pp. 10234029, 1988
“PASSIVE
0042~6989/88 83.00+ 0.00 Pergamon Press plc
SUPPRESSION” BY STABILIZED
OF OPTOKINESIS TARGETS
HARRY J. WYATT, JORDAN POLA and MARCIE LUSTGARTEN ~hnu~acher
Institute for Vision Research, State University of New York, State College of Optometry, 100 East 24th Street, New York, NY 10010, U.S.A. (Received 20 July 1987; in revisedform
7 January 1988)
Ahstrati-Subjects gazed passively at a sinusoidally oscillating optokinetic stimulus. They made no attempt to look at a target which appeared, stabilized on the retina at one of several locations, yet the appearance of the target caused rapid and prolonged suppression of optokinesis. Suppression declined (optokinesis increased) as target eccentricity increased, but could be observed for eccentricities up to 15-2Odeg. We propose that a target moving relative to a background is a stimulus for suppression of optokinesis, depending substantially on the visual properties of the target and not the act of attending to it. Optokinesis
OKN
Suppression
Fixation
Visual stimuli
INTRODUCTION
Optokinetic eye movements are an oculomotor response to movement of a large portion of the visual world; they approximately stabilize the eyes in space (ter Braak, 1936; Jung, 1977; Jung and Kornhuber, 1964; Carpenter, 1977; Robinson, 1981). Since animals with foveas often fixate targets in motion relative to the rest of the world, it is often necessary to prevent optokinesis. We showed earlier that a small target, stabilized on a subject’s fovea, can suppress optokinesis when the subject looks at the target (Wyatt and Pola, 1984). That work did not separate the act of attending to the target (which might in some way “shut off” optokinesis) from the simple visual presence of the target. In the present work, we examined the effect of targets (together with an optokinetic stimulus) presented to subjects who made no e&rt to look at them: even when presented at considerable eccentricity from the fovea, such targets caused suppression of optokinesis. These results were presented in preliminary form at the 1984 Annual Meeting of the Association for Research in Vision and Ophthalmology in Sarasota, Fla.
METHODS
Many of our methods have already been described in detail; here, we emphasize new methods (For further details, see Wyatt and Pola, 1984 and 1987.)
A target (1.5 deg dia.; 0.5 cd/m*) was projected on a rear-projection screen via a high-speed shutter and servomotor-controlled mirror. The target was stabilized on the retina with respect to horizontal eye movements. The optokinetic stimulus field was created with a “planetarium” type projector: holes were drilled in a small drum in quasi-random arrangement; a compact filament-sours at the center of the drum produced pinhole images of the filament on the walls, ceiling, and floor. A typical image had dia. 2 deg and luminance 0.01 cd/m*; average spot density was approx. 1 spot/42 deg’ (average area per spot was a square 6.5 deg on a side). The drum was rotated by a servomotor (Electrocraft), producing horizontal sinusoidal field motion, 30deg peak-topeak at 0.5 Hz. The field motion was made open-loop by adding a signal of eye velocity to the sinusoidal signal frhe motor/drum combination could not fully stabilize the field for saccadic eye movements or fast phases of OKN; drum excursion was about 5&60% of saccade length. We have obtained similar results using closed-loop motion of the field (unpublished results)]. The advantage of the open-loop field is that, during smooth movements of the eye, the average retinal behavior of the field was known. Sinusoidal field motion continued whether or not the target was present. znst~ctio~~ to &jects
1023
Subjects were instructed to remain “passive”
1024
HARRY J.
WYATT
throughout each trial: they were not to attempt to fixate the target or any part of the optokinetic stimulus, but were to gaze ahead; however, they were not to fight any involuntary eye movement that they became aware of. They were to keep their attention at the plane of the wall in front of them, and not gaze into some imagined distance or at an imaginary target. Finally, they were asked to keep their gaze roughly horizontal, which was achieved with little effort (Wyatt and Pola, 1984). Experimental protocol and ~ali~rati5~s
Subjects were dark-adapted for about 10 min before a session. The eye position signal was calibrated and target stabilization checked before and after each trial. At the start of a trial, the target disappeared and oscillation of the field began, After 3-5 cycles of field oscillation, the experimenter initiated the suppression portion of the trial. At the beginning of the next cycle of field motion (max velocity left), the target reappeared at a retinal location randomly selected from a programmed set. The trial continued, the subject remaining passive, for approx. 20 more cycles of field motion. On
PI d.
occasional trials, the pre-target portion of the trial was extended for an additional 20 cycles to obtain more data on the passive optokinetic response. Data recording and ana~~si.~
Eye position (left eye viewing monocularly) was monitored with an infrared system. Stimulus field velocity, and horizontal eye position and velocity were recorded on a polygraph. From 4 set before to 4 set after target appearance, eye vetocity was recorded on disk at 125 samples/set. Steady-state responses (with or without the target present) were analyzed by hand to obtain amplitude and phase lag of smooth eye movements with respect to field velocity. Eye velocity near target onset was studied by removing saccades from the data on disk, and averaging together the eye velocity records (aligned at target appearance) for each subject for each experimental condition. Latency of onset of suppression was estimated by comparing eye velocity following target appearance with eye velocity during the pretarget cycle [An example of onset estimation is shown in Fig. 1 (inset)].
7.5”R
30*/
5
15’
R
C
Fig. I. sample eye velocity records from one subject for three locations of target appearance. The bottom trace shows field velocity (&); other traces show eye velocity (da). At the vertical line marked by an arrow, the target appeared at the location indicated at the right of the record. Saccades have been truncated. Inset: segment of averaged records (saccades removed) for the same subject for the target presented 15 deg right. Solid line shows peristimulus segment; dotted line shows averaged data from the cycle preceding the stimulus. Time scale expanded 3 x relative to remainder of figure; time calibration: 100 msec; open triangle shows estimated onset of suppression.
Passive suppression
Subjects
The subjects consisted of six males and females, aged 2045, emmetropic to 5D myopic, uncorrected. Three of the subjects were naive.
RESULTS
Optokinesis
Optokinetic responses to oscillating fields have been described (Wyatt and Pola, 1984). All six subjects showed vigorous optokinesis, with average velocity amplitude of smooth eye movements 28.7 (SD = 13.3) deg/sec and phase lag 42.9 (SD = 11.4) deg relative to field velocity. (Average gain = 0.61.) Onset of suppression
Figure 1 shows sample eye velocity records from one subject. At the time indicated by the arrow, the target appeared. (Eccentricity indicated at the right of each trace.) It is apparent that suppression appeared rapidly and that it was substantial, even when the target was not on the fovea. The inset shows an example of estimation of latency of onset on an expanded time scale. We performed experiments on five subjects with the target appearing randomly at one of a set of the following locations: fovea1 and 7.5 and 15 deg left, right, up, or down from the fovea. The latencies for onset of suppression were estimated as described in Methods. Since latency was not found to vary systematically with meridian, the results were pooled for each eccentricity. The latencies in msec were: target appearance at the fovea, 150 f 30 SD (range 104-184); at 7.5 deg eccentricity, 186 f 35 (range 120-248); and at 15 deg eccentricity, 246 + 59 (range 168-384). The results in this paper are for targets appearing when the field was moving with maximum velocity leftwards. Pilot experiments showed no systematic difference between this condition and that with maximum velocity rightwards. If the target appeared when the field was at maximum excursion left or right (velocity zero), temporal features of the onset of suppression were difficult to observe [Smooth eye velocity was then low at the moment of target appearance. Also, relative target/field motion at the moment of appearance was zero, and relative motion may be responsible for suppression (see Discussion)].
Suppression in the vector representation
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steady
state-d#erence
The inset in Fig. 2 is a diagram showing how steady-state suppression is plotted. The notation used is based on the “difference vector,” which represents the d@rence that the presence of the target makes in the optokinetic response (Wyatt and Pola, 1984). For purposes of graphic representation, we plot minus one times the difference vector (“-D” in the inset). The basic points to be noted about this representation are that: (i) a smaller vector indicates less suppression; and (ii) a vector that points straight up to 1.0 (i.e. -D being the same as F) indicates perfect suppression (a stationary eye). The remainder of Fig. 2 shows data for three subjects. The target appeared at the fovea, or 7.5 or 15 deg away from it horizontally or vertically (The location 15 deg left was displaced upwards 3 deg to move the target out of the blind spot.) The figure shows that suppression was maximal at the fovea and substantial over a considerable region; however, it decreased as the target moved to more eccentric locations. This fall-off was especially rapid along the vertical meridian for two out of the three subjects shown (We observed this asymmetry for three out of five subjects). We performed further similar experiments using a set of target locations consisting of the fovea and 11 and 22 deg left and right. The two subjects tested still showed considerable suppression for 22 deg target eccentricity [At 22 deg, the lengths of the vectors describing suppression-see Fig. 2-were 0.35 (left) and 0.61 (right) for one subject and 0.71 (left) and 0.66 (right) for the other]. The results described so far were obtained with a target that was considerably brighter than the elements of the optokinetic field (see Methods). To examine the effect of relative target luminance on suppression, we reduced target luminance to match the field elements and ran further experiments of the same type as shown in Fig. 2. With the dimmer target, the latency for suppression became longer and quite variable, and onset was often difficult to pinpoint; however, once suppression developed, the suppression was again found to be considerable and sustained for two subjects tested. Compared to the brighter target, the length of the vector representing suppression (see Fig. 2) was reduced by 0.27 for one subject and by 0.04 for the other (averaged over target positions). Similar
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F
Ldl
Right
I+-- 7.5’--+
Down
Down
Fig. 2. Inset: Diagram of vector notation used to indicate suppression in the steady state. At the left of the inset are the passive optokinetic (F) and suppressed (T + F) responses: length of each vector represents the velocity amplitude of the smooth eye movement (deg/sec), and the angle between the vertical axis and each vector represents the phase lag of eye velocity with respect to field velocity. At the right, the (normalized) difference vector “D” is derived: the passive optokinetic response. (F) is taken as the reference; i.e. its phase lag is set to zero and its amplitude to unity. The suppressed response (T + F) is now scaled in amplitude relative to F, and its phase lag is shown relative to F. The difference vector is then defined as the vector value of F minus T + F, it represents the da@krence that the presence of the target makes in the optokinetic response (Wyatt and Pola, 1984). Finally, for purposes of graphic representation, minus one times the difference vector (,‘-D” in the inset) will be plotted. Note that if -D equals zero, there is no suppression (T + F is identical to F); if-D points straight up to I.0 (is the same as normalized F), suppression is perfect since T + F is zero. This notation also contains phase information: if the vector lies counter-clockwise from upwards, the phase lag of the suppressed response (T + F) was between 0 and 180 deg greater than the phase lag of the passive optokinetic response (F). Clockwise from upwards indicates a phase lag of T + F less than F (or more than 180 deg greater than F). The remainder of the figure uses the vector notation to plot suppression for 3 subjects for various target locations in the steady state. Retinal target location is indicated by the base of each vector.
results were obtained when the luminance of the field components was increased (instead of target luminance decreased) by substituting a tungsten-halogen source for the standard source.
Eflects of attending to a given target location on suppression onset We hypothesize in the Discussion that a substantial amount of suppression occurs without attending to the target; however, it is possi-
Passive
ble that appearance of a target causes a subject to attend to the new target, even without deliberate effort to do so. Such attention could be involved as an intermediate step in producing suppression. To begin examining this possibility, we performed an additional experiment: the same field was used as before and the (brighter) target appeared at 7.5 deg left or right of the fovea. Subjects were told to attend to the right-hand location and push a button when the target appeared there, but to ignore the target (which they were told was “only for a control”) when it appeared at the left-hand location (20% of the time), Onset of suppression was examined for each of the two locations. Figure 3 shows computer-averaged smooth eye velocity data for two subjects: the solid curves are for target appearance at the attended location and the broken curves are for appearance at the “ignored” location. There was no obvious difference in onset of suppression for the two locations; i.e. the task given the subject made no apparent difference in the onset of suppression. DISCUSSION
The results described here indicate that the presence of a target, in relative motion to a stimulus field, suppresses the optokinesis that the field by itself would elicit, even when subjects do not pay attention to the target. It is known from everyday experience that looking at a target suppresses optokinesis to some degree, but previous work differs in assessing the degree. For the case of pursuit against a background, some work has shown a reduction of gain, suggesting incomplete suppression
suppression
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~Collewijn and Tamminga, 1984; Yee ef al., 1984; Barnes and Crombie, 1985); other work has shown a reduction of gain during pursuit initiation, but little or no reduction at later times (Keller and Khan, 1986); some work has suggested an enhancemenl of pursuit against a background (ter Braak, 1957, 1962; Hood, 1975). We have reported that with experienced subjects, steady-state pursuit of an open-loop target against a background shows very little effect of the background (Pola et al., 1983). Using an optokinetic stimulus field and stationary edges, Murasugi et aZ. (1986) observed suppression when subjects attended to the edges, but much less suppression (more OKN) when they attended to the field. In the present work, subjects remained passive; we asked them to continue the same neutral attentional state they were asked to maintain for passive optokinetic responses. We hoped that this would enable us to begin to separate visual from attentional contributions to suppression.
The extent of the spatial domain we observed for passive suppression was impressive: while there was variation between subjects, considerable suppression was observed for eccentricities up to 15 and even 22 deg. In related experiments, Barnes and Crombie (1985) and Murasugi er ai. (1986) found a somewhat more restricted domain: unidirectional OKN was approx. 50% reduced in slow phase velocity when (fixated or attended) targets or edges were 5 deg eccentric. We also found that three out of five subjects showed a horizontally-elongated
1
30’19
1
30*/s
Fig. 3. Experiment to examine effect on suppression onset, of attending to target location. Average smooth eye velocity records arc shown for two subjects. Target onset at the vertical line. Solid lines show responses when target appeared at pre-attended location (7.5 deg R) and subjects responded with a button-pm~; broken lines when target appeared at “ignored” location (7.5 deg L). See text.
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suppressive region. This is intriguing, since the sensitive domain for eliciting optokinesis in rabbits is horizontally-elongated (Dubois and Collewijn, 1979a) which may correspond to the rabbit visual streak (Hughes, 1971) and there is evidence suggesting some elongation of a visual streak even in primates which have predominantly centralized retinas (Stone and Johnston, 1981). In addition to an extensive spatial domain, the speed of onset of passive suppression was considerable: for targets 7.5 deg eccentric and less, the average latency was under 200 msec. Furthermore, the suppression was long-lasting, continuing as long as our trials ran. The increases in latency observed for greater target eccentricities may reflect reduced sensitivity of the mechanism detecting the target (see below).* Relative motion-a
stimulus for suppression?
Our results suggest that, provided with an appropriate stimulus, optokinesis begins to be suppressed quite rapidly, without deliberate effort on the part of the subject. The targets presented here were distinguished from the optokinetic field mainly by being in motion *A possible consideration in these experiments is that the target, by directly obscuring a portion of the field, might create part of the suppression by removing part of the optokinetic stimulation. This is unlikely to be a significant effect for eccentric targets, since a 1.5 deg target at 7.5 deg eccentricity occupies only 2.5% of the visual field between 6.75 and 8.25 deg eccentricity and only 0.8% of the visual field at eccentricities less than 8.25 deg. However, targets at the fovea, while covering only a very small part of the visual field, do cover some of the most sensitive part of the retina for optokinesis (Koerner and Schiller, 1972; Dubois and Collewijn, 1979b; Barnes and Hill, 1984; Pola and Wyatt, 1985). We have carried out some experiments using a foveally-centered target consisting of annuli (either o.d. 1.5deg, i.d. 1.0 deg or o.d. 4.0 deg. i.d. 3.0 deg). Such targets caused approximately the same suppression as the standard 1.5 deg target. which was also approximately the same as the suppression caused by a 4.0 deg dia. disk. We interpret this to mean that a contribution to suppression due to occlusion of the field in our experiments is likely to be minor. tThe one exception was a subject who showed small movements approximately opposite to the field while remaining passive; this subject made vigorous movements opposite to the field when looking at the same target. Thus, the general rule was that the eye movements of a passive subject with a fovea1 target were more like optokinesis-i.e. with the field-than the eye movements of the same subject when looking at the target. The same subject showed movements with the field when passive with an extrafoveal target.
relative to the field (They were also usually brighter than the elements of the field, but a bright target would still act as part of the optokinetic stimulus if it moved together with the field). In a natural visual scene, a target in motion relative to a background is often an object of interest, and its seems reasonable to propose that such a target acts as a “stimulus for suppression” of optokinesis. A mechanism of this type could usefully begin preparation for fixation of the target even before a conscious decision to do so, if the mechanism were fast enough and operated over an adequate spatial domain (which the present results suggest is the case). Visual neurons have been observed with receptive fields which are sensitive to targets in motion relative to a background (reviewed in Allman et al., 1985); similar neurons might provide a substrate for the type of effects described here. When our target was similar in luminance to the field components, the rapidity and strength of suppression was reduced (see Results). As noted above, other work with somewhat similar paradigms found more restricted domains of effectiveness for suppression of optokinesis than we have observed. Assuming that some mechanism must detect the target (or edge) moving relative to the field, then that mechanism might reasonably be expected to detect the relative motion more easily when the target is also distinguished by such attributes as luminance, size, color, etc. [e.g. for targets distinguishable from a background only by motion, peripheral targets must be larger than central ones for detection to occur at the same velocity (Regan and Beverely, 19841. Other factors that may contribute to the extensive domain for suppression observed here are: (i) the fairly low density of texture in our stimulus field; and (ii) the 0.5 Hz optokinetic stimulus we used instead of unidirectional stimuli. Relation of passive suppression to attention
be made clear that there is a the passive suppression described here and suppression while looking at a stabilized target. Subjects actively looking at a foveally-stabilized target against an optokinetic field often move their eyes opposite to the field (Wyatt and Pola, 1984; Pola et al., 1983; Lustgarten et al., 1987); however, subjects who are passive in the same stimulus situation generally show some movement along with the fie1d.t It
should
difference
between
Passive suppression
We did not observe a difference in onset of suppression when we asked subjects to attend to one of two locations of target appearance (Fig. 3). In experiments measuring manual responses to similar target appearances, appropriate cueing of the impending target location can shorten subjects’ manual response times (Posner, 1980); however, whether such findings extend to eye movements is not clear (Klein, 1979). If, as suggested above, passive suppression operates via visual structures sensitive to relative motion, it is possible that it might operate (or operate partly) preattentively, cooperating in setting the stage for the attention/ fixation response.
Acknowledgements-Supported by NSF BNS-8519267. We thank John Orzuchowski for help with the electronics and Wayne Grofik for preparation of illustrations.
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