INFLUENCE OF STIMULUS PARAMETERS ON VISUAL SENSITIVITY DURING SACCADIC EYE MOVEMENT BARBARA A. BROOKS’ and ALBERT F. FUCHS Regional Primate Research Center and Department of Physiology and Biophysics. University of Washington. Seattle. WA 98195. U.S.A. (Received 7 February 1975) Abstract-Visual threshold for stroboscope test flashes was measured during saccadic eye movements over various backgrounds and compared with measures obtained during eye fixation when the same backgrounds were “saccadically” displaced. Amount and time course of threshold change in the two situations compared well, suggesting no necessity for corollary discharge or other oculomotor interferena with primary visual processes during eye movement. No significant threshold rise took place during saccades in the dark. Diffuse test flashes and small well focused flashes were affected differently by specific background conditions. Diffuse Ilashes were perceived with more difficulty during a saccade over a contour-free background than well focused, punctate stimuli. On the other hand. contours in the background raised saccadic thresholds for small stimuli much more than for diffuse test flashes. All threshold changes occurring during saccades were accentuated by increasing the background luminance.

Voluntary saccadic eye movements bring the fovea to new targeti and cause a rapid translation of the entire visual field across the retina. They normally occur many times a minute and during active exploration may happen several times a second. Nevertheless, visual processing proceeds without conscious interruption and the environment remains subjectively stable during saccadic activity. To explain this phenomenon, several investigators have argued for the existence of a central inhibitory or compensatory mechanism whose net effect is to cancel or “suppress” any visual disturbances resulting from the eye movement. This notion has been related to neurophysiological theories of “Efferenz Kopie” (von Holst and Mittelstaedt, 1950) and corollary discharge (Sperry, 1950). Evidence that visual thresholds increase during saccadic eye movement has often been quoted in support of a central inhibitory theory (e.g. Volkmann, Schick and Riggs, 1968). Suppression measured psychophysitally, however, is relative, not total, and experimental descriptions of its strength and time course differ with various investigators. Reported increases in luminance threshold during rapid eye movement over illuminated backgrounds range from about @I log unit (Richards, 1969) to more than 20 log units (Zuber, Stark and Lorber, 1966; see also Volkmann et al., 1968, who describe conditions producing a O-5log unit rise in threshold, which is frequently referred to as a representative value). On the other hand, very intense stimuli given during a saccade are not sup pressed at all (Chase and Kalil. 1972; Michael and Stark, 1966). A near absence of suppression has also been reported during both involuntary (Krauskopf, Graf and Gaarder, 1966) and voluntary (Mitrani, I Please direct reprint requests to: Dr. B. Brooks. Dept. of Physiology, The University of Texas Health Science Center, 7703 Floyd Curl Drive, San Antonio, TX 78284. U.S.A.

Mateef and Yakimoff. 1971) eye movements in dark or dim conditions. When suppression does occur, it is manifest during both large voluntary saccades and the small involuntary microsaccades of fixation (Beeler, 1967; Ditchbum. 1955) as well as passively induced movements (Richards, 1968). The duration of suppression in different studies is also variable, but there is evidence to suggest that it is inversely related to at least one visual parameter, the intensity of the test stimulus (Zuber et al. 1966). In a recent important demonstration, MacKay (1970) challenged the role of eye movements per se in the suppression phenomenon. Using as background a lighted circle upon which was flashed a smaller test spot, he recorded a drop in visual sensitivity for the spot during rapid “saccadic” displacement of the circle when the eyes were fixating. Thresholds were elevated just before, during, and just after the background displacement, with a time course very similar to that associated with actual saccades. This study clearly implicates visual mechanisms in threshold elevations measured during saccades. It also strongly suggests that the visual system does not discriminate between retinal image movement produced by eye movement or by background displacements. Potential neurophysiological correlates are found in several recent experiments which indicate an equivalence, in terms of neural response, between the effects of rapid eye and image movement. Wurtz (1969) provided evidence that cortical unit response in the alert monkey is the same whether the eye moves across the visual stimulus, or the stimulus is drawn across the unit’s receptive. field with “saccadic” velocity during fixation. Similar results were presented for neurones of the cat’s lateral geniculate body and cortex by Adey and Noda (1973), and by Noda. Freeman and Creutzfeldt (1971). Evoked potentials in the cat’s LGB and cortex appear almost indistinguishable whether produced by rapid eye movement or by rapid background displacement while the eye fixates (Jean-

I389

nerod and Chouvet. 1973). Comparable

1973: Ebersole and Galambos. evidence has been offered in

regard to the human lambda wave and is discussed by several authors (e.g. Lesevre and Remond. 1973: Kurtzberg and Vaughan, 1973: Morton and Cobb. 1973). These studies suggest that activity in the visual system during saccades is largely controlled by events at the retina. Sensitivity to test stimuli delivered during eye movement should therefore be regulated by specific conditions in the visual environment. We have investigated some of these conditions. Our first finding confirmed previous results showing almost no threshold elevation during saccades in dim conditions (Krauskopf er al.. 1966; Richards, 1969: Mitrani et al.. 1971) and extended this null observation to include the time just before the saccade. Secondly, we compared measures obtained during background displacements when the eye was fixating to those obtained during saccades over the same backgrounds and found them to be essentially the same, in support

of MacKay’s basic data (1970). Finally, we have looked into the influence of several visual background parameters by testing visual sensitivity during saccades using diffuse test flashes and well focused punctate test flashes. Thresholds for the two kinds of test flash were often independent functions of background conditions, suggesting that at least two systems are differently affected during saccadic activity. In the discussion we attempt to relate these results to general visual function and to some of the previous work on saccadic “suppression”. METHODS Visual sensitivity was tested either in association with a saccadic movement of the eye or a “saccade-like” displacement of the visual background. In most of the experiments. either a punctate or diffuse test flash (1Opsec in duration from a Grass Photo Stimulator unit, model PS-2) was delivered during the course of a movement. Horizontal saccades were measured by the bitemporal d.c. electrooculogram, amplified (Tektronix 3A9 amplifier set at O100Hz). and differentiated to yield a signal proportional to velocity. The upper frequency response of the differentiator was limited by a low pass filter with a time constant of 1 sec. The velocity signal was displayed on an oscilloscope whose d.c. trigger level could be set to occur at various points on the velocity wave form. The horizontal gate then provided a pulse which began with the sweep and served to trigger the occurrence of the test flash. Both the saccade and a signal occurring synchronous with the test flash were displayed on a storage oscilloscope allowing us to time the occurrence of the flash relative to the onset of the eye movement to the nearest 5msec. Almost all saccades were 20” in amplitude and lasted 404Omsec. For horizontal displacements of the visual background, a positive ramp-to-plateau to negative ramp-to-plateau signal was applied to a mirror galvanometer which intercepted the light heam creating the background. The ramps were adjusted to move the background through about 20 in 50 msec causing a constant velocity (4OOdeg/sec) approximating the peak velocities of equally sized saccades (Fuchs, 1971). The ramp signals were processed like the saccades to trigger a test flash during the first third of their trajectory. Test flashes were obtained prior to a saccade by training subjects to execute eye movements in a reaction time paradigm. Subjects exposed to the experimental conditions for

about I5 mm were able to make a saccade helaccn IUC’ fixation points within 12Cl75 msec after the sounding o! a tone. The signal activatmg the tone was displayd and triggered on the “A” time base of 565 Tektronl\ oscilloscope. With the “B” time base in the “starts after ;t delqed interval” mode. the “B” horizontal gate produced ;f pulse occurring an adjustable time after the tone and hence either before. during or after the saccade made in response to the tone. As before. the gate pulse served to trigper the Grass Photostimulator unit. Test flashes were obtained prior to a displacement of the visual background by replacing the eye movement with the ramp signal creating the hackground movement. The variability introduced in the eve movement reaction time paradigm was simulated by ha&g the experimenter’s reaction time to the tone determine the onset of the background movement. As before, the relative occurrence of the flash to either the onset of the saccade or the bachground displacement was measured to the nearest 5 msec by the simultaneous display of the movement and the hash on a memory scope. Procedure

The subject (either the author BB or a naive male undergraduate DB) was seated in a light tight booth facing a translucent tangent screen which subtended 60” vertically by 90’ horizontally of visual angle. The S was dark adapted for at least IOmin prior to all experiments. Backgrounds were projected upon the tangent screen from the side opposite S by means of two slide projectors. One provided a stationary background. or a moving background when a mirror galvanometer was mounted in its optic path. The other projector provided a test flash as described above. The intensity of the flash was controlled by Kodak neutral density filters in the path of the projection beam. The filters were changed between trials by an experimenter standing inside the closed booth near the projectors. Another experimenter monitored the eye movements on an oscilloscope outside the booth. Both experimenters and the S were in contact by headphone intercom. Background luminances were in the upper scotopic and mesopic range as measured by an SE1 exposure meter (England). No lighted part of a given background provided a contrast of more than 2 log units with dark areas of the background. In most experiments. two small fixation points were located on the screen to subtend a visual angle of 20’. If the stimulus were a small spot, it was projected midway between the fixation points but above them by about 15’. thereby ensuring that the fovea would not be stimulated by the test spot during a saccade. The actual retinal position tested depended on when during the saccade the test spot was triggered and in which direction the saccade was going. right or left. Since the trigger time was slightly variable, we deliberately varied the position of the test spot on the screen as a control, thereby sampling an area of retina which included the possible positions on which the test spot could occur under the greatest possible timing variability. Included in this control were deliberate manipulations of trigger time as used in some of the experiments designed to trace sensitivity throughout the saccade. No significant differences were found in the sensitivity of the various peripheral positions tested, nor was the direction of eye movement important. even though one subject (BB) showed a slight consistent difference in saccadic velocity to the right and left. In actual practice, the test flash was reliably triggered during any desired 15msec period of a 20” saccade lasting 6Omsec. At the beginning of a single trial the S placed his chin in a chin rest and was instructed to get ready and then begin making saccades between the fixation points. A comfortable rate was about 1 saccade/scc. After 5-7 saccades the S was instructed to judge whether he had detected

1391

Influence of stimulus parameters the test stimulus (forced choice. yes or no). The judgment was recorded and the routine was repeated until at least five threshold estimates for each experimental condition had been obtained by the psychophysical method of ascending and descending series. Results were very consistent unless the subject was fatigued. On the average. every 12th stimulus was a blank. False positive responses occurred in only 4:’ of such trials. Thresholds during fixation were obtained similarly, except that the S fixated a dark point on the screen while one of the experimenters manually delivered a series of 5-7 single test flashes. after which a judgment was requested. The fixation point was either one of the two target points used during saccades. or one located midway between them. No significant differences were found among the retinal positions thus tested, suggesting that the “band” of retina upon which the test spot might fall in the worst possible triggering conditions during saccades would give uniform results during fixation. We therefore felt justified in comparing measures at any of these three fixation positions to measures obtained during saccades, despite our inability to duplicate the exact retinal position on which the tesf spot fell during saccades. A similar test paradigm was employed when the background was displaced. Ss were instructed to move their eyes and blink frequently between trials to avoid local adaptation and tiring.

Tfrblt!‘I Meetsf nbncontowrcd background luminance on thresholds for a I” test spot. Thresholds at Q5 log ft-L obtained while s’s heads were inside a translucent dome; other values obtained on a 70” x 50” background. The test spot fell approx 15” above the fovea. Luminance is expressed as log ft-L. Thresholds are the reciprocal of the neutral density value required in each particular condition arranged on an inverted scale. Therefore. all threshold values in this paper are on the same relative logarithmic scale. In all tables and figures. A is the difference between movement and fixation thnsholds expressed in log units. and the numbers associated with either the background or the stimulus give its horizontal and vertical extent in degrees of visual angle. Displacement As to be compared with saccadic As are noted by asterisk Subj~sl DB 66

M ,I,%, 0.s

PU

*

D6

sr

b

3.86 2 0.03

6.35 t 0.05

0.49

3.A

2 0.0s

4.U

-+ 0.00

0.39

3.16

f

0.0s

3.37

-* 0.03

co.41

3.06

-+ 0.06

3.36

-+ 0.05

0.32

2.62

-+ 0.07

2.63

-+ 0.02

2.70

-+ 0.01

2.96

+ 0.04

0.26

XT II D* M

-0.21

ix

D6

2.15

-+ 0.03

2.27

-+ 0.06

0.12

2.32

f

0.06

2.36

f

0.02

0.06

1hS

f

0.11

1.A3

-+

0.11

x3

RESULTS

..

The results are presented in seven sections: (1) sensitivity to small, well focused test Hashes during saccades over noncontoured backgrounds; (2) sensitivity to diffuse test flashes during movements with noncontoured backgrounds; (3) the effect of stimulus size during movement with noncontoured backflounds; (4) binocular and monocular tests on noncontoured backgrounds; (5) sensitivity to punctate and diffuse test fiashes during movements with structured backgrounds; (6) time course of threshold change for diffuse and punctate stimuli given before, during and after sac&es; and (7) demonstration of “backward masking” as a consequence of eye movement. In each stimulus condition, the log “saccadic” threshold (measured during either actual saccades or rapid background displacements) is compared with the log fixation threshold and the difference is presented as “A’ in the corresponding tables. 1. Punctute test stimdi backgrounds

(a 1” spot) on noncontoured

In the dark. Very little threshold elevation for a well focused 1” test spot shown 15” above the fovea occurred during saccadic eye movements over dark backgrounds (Table 1). One subject showed an increase of O-09 log units, the other a slight decrease of OG2 log units. Although the entries in Table 1 were obtained for flashes delivered in the first third of a 20” saccade lasting about 6Omsec. additional testing showed that no elevation was present for the interval extending from 100 msec before to 100 msec after the saccade. Repeated determinations of saccadic thresholds in the dark, or in very dii conditions when the fixation points were just barely visible, showed a trend to be slightly higher than fixation thresholds. These differences were usually not statistically signifi-

66 DI

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1.12f 0.10 P -

1.21-+0.12

0.09

0.20

A - 0.19

cant, and a real difference would not exceed a modest maximum of O-1 log unit. Such an elevation may well be due to mechanical stresses at the retina during saccades, as proposed by Richards (1968). Injiuence of background luminance. For all but the lowest background luminance small but significant threshold increases were measured during saccades if the 1” test spot was presented on an illuminated but contour-free background about 70’ wide by 50” high, or if it was focused on a translucent dome fitted over the Ss head to provide an entire contour-free visual field (Table 1). The difference between thresholds with eyes fixating and saccading increased with background luminance but was never more than about 05 log units in our conditions. The increase in A with background luminance is similar to that described by Richards (1969). and is plotted in Fig. 1 (dotted line). While there is no immediate explanation for this effect, it seems primarily to be visually mediated since displacement of the same background during fixation elicited a very similar threshold increase (Table 1). All of these observations apply as well to a single vertical stripe stimulus. I” x 25”, regardless of the fact that the stripe fell on the fovea during fixation and possibly sometimes during saccades.

BAHI%.~K~A. BMKKS and ALU~RT F. F.r CHS

I .3’)2

Table 1. Effects of noncontoured background lummancc on thresholds for a diffuse test flash. Details as 111Tabic ! SUbjLCC

Bdi.m (106 FL)

DB

A

Fix

6.C

3.A5 -+ 0.04

A.83 -+ 0.06

1.38

3.55 I+ 0.03

4.79 _+ 0.03

1.24

2.78 + 0.07

4.02 -+ 0.0s

1.24

2.91 -+ 0.04

3.97 -+ 0.04

1.06

2.46 -+ 0.06

3.41 -+ 0*05

+0.95

2.39 I+ 0.01

3.09 -+ 0.05

0.5 4 6B

DB c5 IIB

DB iTT

1b Dotk

BB

’’

@5

i% Bockground L~i~nce

CC5

no.60

0:s

( logf t-t!

Fig. I. Threshold elevation (A) during saccadesfor diffuse test flashes (closed symbols. continuous line) and I’ spot flashes (open symbols. interrupted line) as a function of noncontoured background luminance (abscissa marked off in measured ft-L values). Data from subject BB as circles: from subject DB as triangies. Square shows averaged data from four student volunteers. Curves hand drawn.

_. 1 “Full fielrf’ grounds

test stir&’

on noncontoured

back-

There was no reason a priori to expect visual sensitivity during eye movements to be different for small test stimuli than for large test stimuli. It was therefore surprising to find consistent differences between the amount of threshold change for spot and full field test flashes, even when the backgrounds were identical. The one common feature for large and small test stimuli was the lack of significant threshold elevation on a dark background. The increase in threshold for the detection of a large flash in the dark was DO8 and @I 3 log units for the two subjects. When thresholds were tested during eye movements made over noncontoured backgrounds at the highest available luminance, a threshold increase of about 1.3 log units was recorded for the diffuse flash. while that for the spot did not exceed 05 log unit (compare Table 1, top row with Table 2. top row). When the actual threshold values are compared it can be seen that about O-6 log unit more luminance was required to detect the diffuse flash than the 1” spot, even though the @ation threshold for the diffuse flash (about 3.5 log units) was lower than that for the spot (about 3.8 log units), as might be explained by a spatial summation effect. This seemingly paradoxical requirement of more luminance for detection of diffuse flashes than spots during saccades generally held when background luminance was present. As with the small test spot, threshold elevations for the diffuse flash increased with background luminance. Figure I graphically demonstrates that threshold elevation for a diffuse flash during saecades is always more marked than for a spot stimulus (continuous line). Once again, saccadic elevations were reliably mimicked by displacing the background (compare saccade As of 040 and 095 with displacement As of 0.79 and 0% respectively). Althou~ the large rectangular backgrounds projected on the screen and the translucent dome were as homogeneous as possible. there was an average

luminance gradient of approx 04 log unit from center to edge of the rectangular background, and also one of about @3 log unit from central fixation position and far edge of the visual field inside the dome. These differences should be kept in mind when evaluating the results. 3. Stinuilus area The above observations suggesti that the amount of threshold increase during saccades was related to stimulus area. In Fig. 2 threshold elevation is plotted as a function of stimulus diameter for saccades made over two different noncontoured backgrotm& one of moderate (m log ft-L) intensity and the other dark enough so that the two fixation points could barely

Siimulu; Fig. 2. Effect of test stimulus size (diameter) on threshold elevation (A) during 20” saccades. Background noncontoured and rectangular (75” by 60”) except for result with stimulus dia of 2.2 log degrees in which the ‘dome’ baekground was employed. Open symbols: background = m log ft-L. closed symbols: background = n log ft-L. One standard deviation representedby the vertical tine- through data points. Circles for subject BB. triangles for subject DB. Curves hand drawn.

1393

Influence of stimulus parameters

be made out against the screen (n log f&L). Clearly, the threshold elevation increases on either background as the diameter of the circular test spot grows. Furthermore. while no threshold increase was measured for small spots against the darkened background, significant elevations were seen if the test spot exceeded about 6” dia. suggesting that the large test Hashes are particularly affected by scotopic conditions. In order to demonstrate a lack of elevation for large test flashes in the dark (Table 2) it was in fact necessary to take extreme precautions against stray light in the visual field. Optical restrictions precluded reducin spot size below about O-75’ so that the curve for the $1. log ft-L background in Fig. 2 is incomplete. The difference between the two curves indicates that higher background luminance not only increases threshold elevation for a given spot size, but also decreases the diameter at which a noticeable elevation occurs. The saccadic threshold elevation was similar for a stripe 1” wide and 25” high as for a 1” spot in all conditions in which the two were compared. (A values may be compared between Tables 1 and 5 for noncontoured backgrounds, and between Tables 4 and 5 for contoured backgrounds.) The subjects’ reported perception of the full field test flash was different than for a spot or stripe. Small spots and stripes were detected as well focused entities, whose perceived location in the visual field was often affected by the saccadic movement (see Matin and Matin, 1972). Diffuse flashes, on the other hand, had no location and were perceived simply as a disturbance in ambient luminance. Possibly, sharp borders or even the spatial harmonic components of the spot and. stripe stimuli were more important than area in setting the saccadic threshold. Such features have been found relevant to differences between flicker (or flash) detection thresholds and pattern recognition thresholds in the fixating eye (see Tolhurst 1973; Kuiikowski and Tolhurst, 1973). Another possible explanation for the dependence of saccadic threshold on stimulus area concerns movement of contours over the peripheral retina. Such contours were present both at the edges of our projection screen and when the subject was inside the dome. Subjects become quite conscious of the orbit of the eye and of nose and eyebrow contours while being tested in the dome. To the degree that these contours always affect the retina when there is ambient luminance, the visual field is never perfectly “homogeneous”. During an eye movement there is considerable shift of “orbital shadow” on the retina and it is conceivable that such shifts affect thresholds for stimuli whose borders come near retina affected by the orbital shift. Thus, large circular stimuli might be more affected than small spots in the center of an otherwise pattern-free visual field. We do not favor this kind of explanation, at least without further testing, for two reasons. First, intentional projection of stripes onto the whole background hardly affected the saccadic threshold for large test stimuli, as long as the overall level of luminance was held constant (see Tables 4 and 5). This finding is difficult to reconcile with the notion of spatial spread of effects from shifting borders or contours in the field periphery. Secondly, in control

tests we found that the amount of threshold rise for a spot stimulus was the same regardless of whether its retinal test area was close to or far away from areas affected by shifting borders. A spot could be projected 2-3” away from a retinal area affected by orbital shadow shift, or any other pattern or contour shift, and the amount of threshold increase during a saccade remained the same. Thresholds during saccades were altered only when the retinal test area was directly affected by the pattern shift (see Fig. 4). When the test spot was moved to various retinal locations which more or less corresponded to the periphery of a circle. radius 25”, centered on the fovea, it was possible to determine that the position of the test spot did not affect the amount of threshold change during a saccade as long as the retinal test area was not directly affected by pattern or luminance shift. We therefore concluded that there is probably little significant spread of effect from shifting borders during an eye movement. regardless of whether such shifts are induced extra- or intraretinally. It is our current opinion that saccadic thresholds for 1” test spots and for full-field test stimuli projected on a “pattern-free” background are probably determined by a sensitive retinal mechanism which registers diffuse shift of luminance at the retinal test area caused by the saccade itself. This mechanism may have a “receptive field” which is sensitive to test area or size, thereby relating to the results of Fig. 2. 4. Monocular and binocular tesestson ttoncontoured backgrounds

Dichoptic presentation of background in one eye and test stimulus in the other would offer evidence as to the central-peripheral site of interactions responsible for the threshold increases during saccades on noncontoured backgrounds. This presentation was technically unfeasible in our present setup, but we were able to demonstrate that the effect is at least not dependent on interocular interaction, since it is equally strong in both monocular and binocular conditions. Table 3 shows data obtained for two stimulus sizes presented against a noncontoured background. One eye was occluded with black masking tape for the monocular tests. Instead of a diffuse stimulus we selected one 20” wide and 40” high and projected it in the center of the background, which was 70” wide and 60” high. Since the eye movement was 20” in amplitude, this arrangement insured that the borders of the background would not encroach on retina receiving the test flash during the saccade. The test Table 3. Monocular and binocular thresholds on a noncontoured 70” x 60” background for two test sizes, a I” spot and a 20” x 40” rectangle. Bd luminance = m log

ft-L. Data from subject BB 10 wr liX -

3.09f 0.05

sac-

3.24 f 0.04

b

200x 600 2.67f 0.w

0.94

0.15

Ilxbimc

2.91 -+ 0.07

Sac bin=

3.13 -+ 0.05

h

3.61 f 0.04

2.46 f 0.02 0.95

0.23 3.41 -+ 0.05

139-l

BARBAKAA. BROCXSand ALBERTF. FL CHS Table 4. Difference (A) between fixation and saccadic thresholds on several backgrounds. for both spot and diffuse

stimuli. Luminance of light parts of all fields was 0.5 log ft-L, and total illuminated area was the same in conditions B. C ;Ind D Data rrom DR. scti

6

Bd

1.&3

Diffuse A

Dose 0.12

Spot

Diffiee B

Cheekend field 750 x 500

Diffuse

Striped

79

C

fiald x SW

1.62

Diffuse u&t Spot

1.02 2.18

Spot

D

1.70 2.06

spot

"tram"* 0.22

flash was large enough so that further increase of its area would not affect its saccadic threshold measures on this background (i.e. the saturation effect in Fig. 2). Likewise according to Fig. 2, the spot could be expected to show significantly different saccadic thresholds (by about 0.7 log units) than the larger stimulus. Table 3 indicates that the dzfirence between thresholds obtained during fixation and those obtained during saccades is not dependent upon binocular mechanisms for either the large or the small test flash, since the threshold elevation is almost identical whether in monocular or binocular conditions. The difference in threshold elevation between the binocular and monocular conditions was 0.08 for the spot and 041 log units for the large flash stimulus. Table 3 also shows a small binocular facilitation for all thresholds, between 01 and 0.2 log unit, which occurs for both the small stimulus and the larger one. Once again, the larger stimulus requires less luminance than the spot to be seen during fixation, while during saccades the converse is true. 5. Comparison of diffuse and punctate stimuli on structured backgrounds

Our previous data have demonstrated that large noncontoured backgrounds affect the detection of diffuse flashes more than small spots; this section will show that contours in the background strongly depress sensitivity to punctate stimuli while having relatively little effect on diffuse flashes. Table 4 depicts threshold increases for diffuse and spot stimuli during saccades over various backgrounds of roughly the same average luminance, but very different distributions of luminance. Threshold values and standard deviations have been omitted for clarity since they differed in no way from others in this paper. Saccadic threshold elevations for the two stimulus types are seen in the A column. Data in row A represent the noncontoured condition; in rows B and C the test spot was shown on either a 2” dark stripe of a dark-light striped background (C) or a

dark check of a checkered background (B). Agam the test spot was positioned 15’ above the fixation pomts. Against either the checkered or striped background. the saccadic threshold for the spot rose more than 2 log units compared to about 0.4 on the noncontoured background. In contrast. the threshold for dlffuse flashes during saccades were only moderately increased on the contoured background [from 143 to either I.70 (checkered field) or 1.82 (stnped field)]: contours added only about 0.4 log unit to the increase already attributable to the noncontoured background (i.e. 143 log units under the dome or the 1.61 log units due to a light frame). In row D the background luminance was redistributed as a “frame”. leaving a rectangular central area roughly 35’ high and 50’ wide and approx I.5 log units darker than the frame itself. In this condition the spot was presented against a darker but equally as noncontoured background as in row A. and its threshold during saccades rose only 022 log unit. Threshold increases for the diffuse stimulus on the other hand was 1.61 log units. a value not greatly different than that for the striped (1.82), checkered (1.70) or noncontoured (1.43) backgrounds. These results suggest that detection of punctate stimuli is much more regulated by contour in the visual field and that detection of diffuse test flashes is more affected by the average luminance. An experiment was specifically designed to detail these differences. Table 5 shows data obtained on two backgrounds for a middle-sized test flash compared with a single stripe test flash. Fixation threshold for the larger stimulus on the noncontoured background was less than that for the stripe by 0.2 log unit. During saccades over this background the threshold for the larger stimulus rose by 0.96 log unit. while that for the stripe increased by only 0.33 log unit. The larger stimulus required almost 0.5 log unit more luminance than the spot in order to be seen during a saccade. A 0.3 log unit neutral density filter was subtracted when the background was composed of dark and light stripes to give an overall luminance rough11 equal to that of the noncontoured field. Against the stripes, the fixation threshold for the large stimulus decreased by about @2 log unit compared to its value on the noncontoured field of the same average luminance. This may be due to the fact that the flash was prqiected tltrowgh the screen. and its contrast was greater on dark than on light stripes. Whatever the reason. it was perceived as a “vaguely centered” disturbance in ambient luminance, its edges not being evident. Fixation threshold for the stripe stimulus decreased in comparison to its value on the noncontoured background by only about 0.07 log unit, even though it was projected on a “dark” stripe which was 1.2 log units darker than the noncontoured background. This stripe threshold, however, is determined during fixation not only by background luminance. but by the proximity of other stripe borders on its right and left side (Brooks and Fuchs, in preparation). The stripe threshold increased by 2.15 log units during a saccadic eye movement over the striped background. as compared to its fixation value. This difference is so large as to preclude any explanation based on changes in effective luminance levels caused by the saccades. The actual saccadic threshold was

1395

Influence of stimulus parameters Table 5. A comparison of thresholds for strip

and diLse stimuli on a noncontoured and a contoured background. Luminance of light stripes was 1.0 log R-L. A Q3 log unit filter added to the noncontoured field equated total luminance in both conditions

2.43 i

3.90 -+

0.03

0.03

4.92 log units a value far in excess of either the flxation (244) or saccadic (3.17) threshold on the noncontoured background field of qual luminance. Hence

there must be a mechanism comxcted with the presence of contour which contributes at least 75% of saaadic thrtshold increase on the striped background. Once again, the effect of rapid displacement of the striped background on the detection of the

large or stripe test stimulus was a threshold increase of 1.29 and 2.27 log units respectively; this compares favorably with the threshold increase of 1.37and 2.15 log units due to a saccade over stationary stripes. 6. Time course of sensitivity decrease during saccades and during background displacement

Measures described above have shown that the amount of threshold rise during saccadic diilacement of the background compares well with threshold changes during real saccades over similar back-

80

-50

o_

100

200

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Fig. 3. Time course of change in visual sensitivity for 1” light stripe tlashed against a striped background at three different intensities (04, 1.6 and 22 log units above fixation threshold for the test stripe against a dark hackground stripe). Visual sensitivity is measured as frequency of seeing the test stripe in per cent. Average duration of a 20” saccade or target displacement whose onset is at zero time is represented by the calibration mark. Open circles for subject BB. closed triangles for subject DB. Details in text.

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grounds. In this section we will present evidence that the time course of “suppression” is also similar in the two situations. In addition it will be seen that the time course of decreased sensitivity is a function of the intensity of test stimuli; intense stimuli are perceptible during the whole course of the eye movement or displacement. In this serieq a test flash of constunt luminance was provided at various times relative to the onset of a movement and the subject judged whether it was present or not. By combining a large number of single judgments into time biis before, during and after a displacement or saccade, the percentage of test llashes seen could be plotted as a function of time. In Fig. 3 the frequency (“A)of seeing (i.e. visual sensitivity) for a 1” test stripe &shed against a striped background was plotted for three test conditions. For the broader curves (low intensity), the constant test intensity was set at 04 log unit above the fixation threshold for the test stripe against a 2” black stripe of the background. This intensity fell below the saccadic and displacement thresholds of the striped background by about 1.6 log units. For the narrow curves (medium intensity), the intensity was increased by 1.2 log units so that it was only 04 log unit below movement threshold. For the flat curve at the top of the figure, the test flash was set at 02 log unit above movement threshold. It was of course seen all the time, and the curve is included for illustrative purposes only. Although the curves were from different subjects or measured on different days, the time courses for saccadic eye movement and background displacement are remarkably similar. Sensitivity decreased to low intensity flashes presented both before the saccade and before the background displacement; furthermore, the decrease persisted for up to 2OOmsecafter the termination of either movement. In contrast, at any time near the movement, medium intensity flashes were perceived far more frequently, and the time course of suppression was much shorter than for the weak stimuli. The curve for the medium stimulus shows recovery during both saccade and displacement (see related curves in Zuber et al., 1966).

The same trend for relatively strong stimuli to produce narrow and shallow time course curves was aiso noted for large test flashes presented agaainst noncontoured backgrounds. Likewise. large test flashes which were relatively low in intensity (close to fixation threshold) resulted in broad. deep time course curves with noncontoured movement. Since these data are in principle the same as those depicted in Fig. 7 for a contoured background. they are not illustrated.

Increases in threshold for stimuli delivered before a saccade are frequently used to support the existence of a central inhibitory mechanism (Volkmann CI ~1.. 1968). An alternative explanatjon to a centra1 inhibitory signal of oculomotor origin is that neural signals reporting a dim test flash travel slowly, and are overtaken and suppressed by faster signals resulting from the saccadic dislocation of the visual environment. This sequence of events would constitute the well known visual phenomenon of “backward masking” (see Kahn~man. 1968). For example. backward masking has been invoked to explain the increase in luminance threshold measured in a fixating eye just hqfire the onset of a conditioning background (Crawford. 1947; Baker, 1949). The experiment described here (Fig. 4) sets conditions which result in an increase in threshold for a test flash delivered before the responsible lummance changes are produced by a saccade. In Fig. 4. a test spot always occurs 3” into the dark half of a light-dark visual field. The fixation threshold for the spot when the ‘field center was fixated was 2.40 relative log units; during the sacfade from right to left fixation points it rose to 362 log units. an elevation of 1.22 Iog units. (We11 after the saccade was over, the fixation threshold for a spot on the Iightrd half of the field was 3.31 log units.) The 1.2 log unit saccadic rise could be due to a “backward mask” of light for the retinal area stimulated by the test spot, since the retinal locus of the test spot is covered with light shortlv after the occurrence of the test flash. When the en&e central visual field was dark, threshold increased by only 0.17 log unit. The timing for the occurrence of test flash and saccade is complicated; it is detailed for reader convenience in the legend of Fig. 4. The consequence of the left-to-right eye movement was to remove light from the retinal locus of the test spot shortly before the test spot was flashed (see Iegend of Fig. 4 for details). Under these conditions. the saccadic threshold rose to 2.87 log units, an elevation of only 047 log unit over the fixation threshold of 240. In summary, the threshold elevation under conditions favorable for backward masking (i.e. right-to-left saccades) is greater by at least 075 log unit than saccades which did not provide such conditions. These findings suggest that the threshold for the test spot during eye movement was dependent not on the background on which it was actually flashed. but on changes at the retinal test area provided by the shift in visual field. While these measures did not involve test flashes given before the saccade itself. we feel that the point is adequately made that threshold is affected even if the shift occurs qftw the test flash is shown.

Fig. 4. A detailed account of the events accompanying a saccadic eve movement over a half dark. half light background. 66’ wide and 40” high. Lighted background = m log ft-L. darkened background = 2.0 log R-L. The task was to detect a spot flashed on the retina from the “asterisked” position in the visual field (column B). The trigger level of the 20’ saccade was set so that the spot occurred about midway through its total trajectory. The half circle with the open arrow represents the retina: the solid black spot is the retinal location (retinal test area, RTA) upon which the test snot wilt appear; the stippled annular sector represents the retinal image of the dark area of the visual field. Crosses represent fixation points. A saccadic eye movement from the right to left fixation point (starting in column a) across the visual field will have the following consequences: (I) the RTA is originally covered by the dark portion of the background (a); (2) at the middle of the saccade (b). the test spot is ignited and falls on the RTA still covered by the dark portion of the background; (3) shortly afterward, the RTA crosses the dark-light border (b to c); (4) after which the retinal test area will be covered with light for the remaining part of the trajectory and for the duration of the next fixation (c), a period of about 1sec. On the other hand, an eye movement from the left to the right fixation point (bottom row) will cause a light spot activated half way through the saccade to occur on a retina) area which ltad been illuminated during the previous fixation, but was crossed by the border (luminance was removed) just br?fore the spot was flashed.

The effect was very similar when the visual field was displaced during fixation. DISCtJSSlOlr;

One of the principal results of this study confirms previous reports on the lack of significant threshold elevation during saccades made in the dark (Krauskopf et al.. 1966; Mitrani er al., I971 ; Richards. 1968). Although a threshold increase up to 0.1 log unit was occasionally measured in the dark, we ascribe this elevation to a nonvisual, nonoculomotor source such as the retinal shearing forces due to vitreous inertia as proposed by Richards (1968). Significant threshold elevation in the dark reported in other studies may be related to uncontrolled stray light. Another conclusion possible from these experiments is that the visual system reacts similarly during background displacements and during saccades. Both methods of image displacement have comparable effects on visual thresholds; furthermore. the time course of threshold elevation is the same, including the elevation to test stimuli delivered before the onset of the movement (first pointed out by MacKay, 1970).

Influence of stimulus parameters

Similar conclusions regarding slower .image displacement and pursuit movements were recently reported by Tolhurst and Hart (1973). The comparable consequences of eye movement and background displacement severely challenge the necessity of a “corollary discharge” or other central mechanism with inhibitory properties, at least in relation to the kinds of visual detection processes with which we are dealing in this paper. A corollary discharge might nonetheless have functions other than the suppression of visual sensitivity during eye movements (MacKay, 1973). Our most interesting result from the point of view of information processing during normal eye movement is the indication of independent processing for well focused punctate stimuli and diiuse test gashes during eye movement. Although a diffuse test flash is perceived more easily than a small stimulus during fixation on a contour-free background, quite the opposite is true during rapid eye movement. The process governing saccadic sensitivity to large test flashes functions at scotopic levels where punctate stimuli are little influenced (Fig. 2); since saccadic sensitivity to large gashes is relatively unaffected by the distribution of pattern in the background, we might suspect a strong influence from the retinal periphery. Ah of this suggests that the diffuse flash detection mechanism is sensitive to the rapid shifts of diffuse luminance affecting large areas of the retina which may occur as a result of eye movement. Such a system, sensitive to “saccadic” shifts of diffuse luminance, might be refractory to additional ambient or diffuse stimulation as provided by our large test flash in close temporal proximity. While these speculations apply to the case of a diffuse test stimulus, we have shown that patterns in the background which little influence large test flashes have considerable effect on the detection of small spots or stripes during saccades although these stimuli are little affected when presented on a relatively uniform background. The mechanism by which this is accomplished is not at all clear. More than 75% of the threshold rise for a spot or stripe observed during a saccade over the contoured backgrounds in this paper is unexplained when compared to the threshold on a non-contoured background of the same average luminance (Results, section S), signifying that the spot is not merely perceived against a “blurred” background. Some dynamic process is called into play as a result of a saccade or background displacement involving contours, and our preliminary observations suggests that the retinal locus of the test spot must be directly affected by the background contour-i.e. that there is little spatial interaction in this effect. It is tempting to relate these observations to recent studies which suggest independent movement-flicker and pattern detection “channels” operating in the fixating eye (e.g. Keesey, 1972; Tolhurst. 1973; Kulikowski and Tolhurst, 1973). It is interesting that such data are accumulating, not only in psychophysics but also in neurophysiological investigations (see for example Singer and Redworth, 1973; Stone and Dreher. 1973; Maffei and Fiorentini, 1973). We have not attempted to relate our findings in detail to all of the other studies of sacmdic suppression which have taken place in a wide variety of ex-

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perimental conditions. Some workers have themselves questioned the source of small amounts of threshold rise measured in well controlled conditions (e.g. Volkmann. 1962: Volkmann et al., 1968). Our study shows that at least three factors must be kept in mind when evaluating “suppression”: (1) overall background luminance; (2) test stimulus size and possibly focused edges; and (3) possible interference at the retinal locus of a contoured test stimulus of background contours or luminance shifts. It is likely that the divergence in quantitative estimates of threshold among authors is partly because these factors were uncontrolled. Ack,towledgernerztshis investigation was supported in part by National Institutes of Health grant RR00166 to the Regional Primate Research Center. by National Institutes of Health Special Fellowship EY54407 to Dr. Brooks. by a research award from the National Society for the Prevention of Blindness and by PHS grant No. ROI. EYOO745-03to Dr. Fuchs. The authors gratefully acknowledge the assistance of Mr. Carl Case and Mr. Don Bliss.

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