Electroencephalography and Clinical Neurophysiology, 1977, 4 3 : 8 2 5 - - 8 3 6

825

© Elsevier/North-Holland Scientific Publishers, Ltd.

AN OBJECTIVE INDICANT OF B I N O C U L A R VISION IN HUMANS: SIZE-SPECIFIC I N T E R O C U L A R SUPPRESSION OF VISUAL EVOKED POTENTIALS * M. RUSSELL H A R T E R , VERNON L. TOWLE, MARIA ZAKRZEWSKI and STEPHEN M. MOYER

Department of Psychology, University of North Carolina at Greensboro, Greensboro, N.C. 27412 (U.S.A.) (Accepted for publication: May 3, 1977)

The visual system contains channels selectively tuned to patterned stimuli of various spatial frequencies or element sizes. This has been demonstrated in man psychophysically (Blakemore and Campbell 1969; Blakemore et al. 1973) and electrophysiologically (Campbell and Maffei 1970; Musso and Harter 1975; Mecacci and Spinelli 1976) by showing that adaptation or masking with a given spatial frequency reduces responsivity to that specific spatial frequency b u t not to spatial frequencies removed by two octaves or more. Three studies have shown that this size-specific suppression transfers interocularly in subjects with normal binocular vision. Maudarbocus and R u d d o c k (1973) adapted one eye for 3 min with varying spatial frequencies and then psychophysically measured contrast sensitivity to a given spatial frequency presented to the other eye. Abadi (1976) varied the difference in dichoptically presented spatial frequencies and psychophysically measured suppression rivalry threshold. Harter et al. (1976) continuously presented various spatial frequencies to one eye and simultaneously recorded visual evoked potentials (VEPs) to a given spatial frequency flashed to the other eye. In these studies, the greatest interocular

* Portions of these data were presented at the American Academy of Optometry, Miami, Florida, 1974 and the Association for Research in Vision and Ophthalmology, Sarasota, Florida 1975. This research was supported in part by a Sloan Foundation Grant and a UNC-G Institutional Grant.

suppression was noted when identical spatial frequencies were presented to the t w o eyes, progressively less suppression being obtained as the difference in spatial frequencies presented to the t w o eyes was increased. These data indicated the subjects had central binocular channels which were tuned to specific spatial frequencies. This conclusion is further supported b y data from simple striate cells of cats which indicate spatial-frequency specific adaptation (Maffei et al. 1973). The hypothesis tested in the present study was that subjects with p o o r binocularity, as measured by stereoacuity, would show reduced size-specific interocular suppression of VEPs. This hypothesis was based on evidence indicating that animals with disrupted binocular vision have fewer binocular innervated cortical cells (Hubel and Wiesel 1965; Wiesel and Hubel, 1965), that humans with poor stereopsis show reduced interocular transfer of the tilt aftereffect (Movshon et al. 1972; Mitchell and Ware 1974), an effect attributed to the loss of binocularly innervated cells, and that preliminary data suggest an amblyopic eye does n o t interocularly suppress the macular response of the normal eye (Spekreijse et al. 1972). If this hypothesis should be supported, VEPs could be used as an objective indicant of the presence and degree of binocularity. A secondary purpose was to assess the effects of stimulus intensity on the interocular transfer of size-specific effects and whether differences in stimulus intensity

M. RUSSELL H A R T E R ET AL.

826

might account for such transfer in one previous study (Harter et al. 1976) but not in another (Harter et al. 1974).

STIMULI EYE FLASHED 1.5 LOG UNITS

Method

Subjects Twelve students or faculty participated in the experiment. Their visual characteristics (Table I) were assessed with a Bausch and Lomb Orthorater (resolution visual acuity, stereoacuity, lateral phorias), a Howard--Dolman Depth Perception apparatus, and visual sighting tests of eye dominance. All subjects had monocular visual acuities better than 20/ 67. Subjects were divided into two groups, those with 'Good' and those with 'Poor' binocular vision, on the basis of their performance on the Orthorater stereoacuity and Howard--Dolman depth perception tests (as measured in average Z-scores). These two measures of binocularity were correlated (r = +0.79, P < 0.001). With the exception of one subject (Li), the Poor Binocularity Group had stereoacuities worse than 19 sec of arc. Four of the subjects had previous experience in the laboratory, three of which were in the Good Binocularity group. Visual stimulation Obliquely oriented crossed line grids, reproduced on transparency film, were used as stimuli (Fig. 1). The transparencies consisted of white lines on a black background (ratio of widths 1 : 7) and subtended 7.6 ° in height and 10.2 ° in width. The size of the pattern elements or squares, as measured by the subtended visual angle between line centers, was 15, 30 and 60 min of arc. The fourth stimulus consisted of a neutral density filter with luminance transmittance equal to that of the grids. Independent stimulation of the left and right eye was achieved by means of a haploscope (Harter et al. 1976). The transparency viewed by one eye was continuously back illuminated with a 150 W incandescent light bulb, the luminance transmittance through

EYE CONTINUOUSLY ILLUMINATED { 0.38

OR 38.0 m L )

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Fig. 1. Example of stimuli haploscopically presented to the flashed and continuously illuminated eye. The patterns were negative transparencies (white lines on a black background). Numerical values beneath each pattern indicate square sizes in the grids in subtended distance between line centers.

this transparency being either 38.00 mL or 0.38 mL. The transparency viewed by the other eye was in darkness except when back illuminated by a 10 psec flash once every 725--1725 msec. Flashes were produced by a Grass PS-2 photostimulator and were 1.5 log units above absolute threshold for the stimulus conditions (as determined by inserting neutral density filters in front of the flashes until they could not be detected by the subjects). The grids were viewed through 1 mm artificial pupils and were presented to the two eyes spatially out-of-phase. The latter minimized the confounding of correspondence of points of retinal stimulation with the similarity of the grid sizes viewed by the two eyes, the lines viewed by each eye falling on disparate retinal points in all conditions. This stimulus paradigm enabled the investigation of interocular suppression of monocular VEPs to 15 or 60 min of arc grids flashed to one eye, the flashed or test eye, as a function of the intensity (0.38 or 38.00 mL) or square size (diffuse light, 15, 30, or 60 min of arc) o f the grid continuously viewed by the other

INTEROCULAR

S U P P R E S S I O N O F VEPs A N D B I N O C U L A R I T Y

827

TABLE I Visual characteristics of subjects with good and poor binocular vision Key to notations: a, Binocular depth perception measured by Howard--Dolman apparatus (error measure: standard deviation in ram); b, Stereoacuity: Fry--Shepard scale (sec); c, "a" and " b " above were converted to z-scores and averaged; d, F-ratios indicating magnitude of interocular suppression due to grid size presented to the "suppressing" and "test" eyes. Poor (experimental group)

Subjects

Ar Binocularity • H.D. a Stereo. b

4.53 0 (362") ** --1.74

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De

3.60 0 (362") --1.38

Mi

3.31 0 (362") --1.26

1.18 17.8 (362") --0.23

Ge

Li

2.82 76.5 (43") --0.21

2.46 96.0 (19") 0.16

0.7 0.7

1.0 1.0

0.9 0.3

1.1 0.9

1.2 1.2

0.8 1.0

--4.5 210--230

+6.0 170--190

+7.0 220-240

--9.0 220--230

+3.0 190-210

+6.0 220--240

5.6 9.1 7.4

3.3 5.5 4.4

0.1 10.9 * 5.5

1.4 4.7 3.1

4.5 6.3 5.4

2.5 5.7 4.1

Good (control group)

Binocularity H.D. a Stereo. b Z~ Visual acuity Left eye Right eye Lat. Phoria (A} VEP ampl. measure latency (msec) F-ratio VEP ampl. d Sup. Test X Suppl. X * F(0.05) = 9.28,

Sa

df: 3,3.

Ma

Ve

Ru

Ri

Su

St

1.37 106.5 (9.7") 0.70

1.25 106.5 (9.7") 0.75

0.92 96.0 (19") 0.76

0.64 96.0 (19") 0.87

0.81 106.5 (9.7") 0.92

0.49 106.5 (9.7") 1.05

0.9 0.9

1.2 1.2

1.2 1.2

1.2 1.1

1.2 1.1

1.0 1.1

--3.0 180--200

0 160--170

0 170--200

--3.0 150--180

--3.0 230--250

--4.5 230--250

7.1 13.0 * 10.0 *

1.8 1.0 1.4

100+ * 93.1 * 96.5+ *

15.2 * 8.8 12.0 *

14.7 * 19.7 * 17.2 *

62.5 * 78.5 * 70.5 *

** " sec of arc.

eye, the continuous or suppressing eye. Both eyes were never stimulated for a sufficient duration for rivalry to develop (due to the brief nature of the flashed pattern).

Experimental design The conditions presented to the left and right eye were varied in the following order: A grid w a s f l a s h e d t o o n e e y e f o r s u c c e s s i v e b l o c k s o f 32 f l a s h e s , e a c h b l o c k c o n s i s t i n g o f

828 continuous presentation of either diffuse light, 15, 30, or 60 min of arc squares to the other eye. This series was repeated in an ABCD, DCBA series, each condition being presented a total o f 64 times and resulting in one averaged VEP. This series was repeated in a counterbalanced order until all remaining conditions were presented to b o t h eyes. The order of presentation of conditions was also counterbalanced across a second replication and across the six subjects within each binocularity group. The effects of binocularity (Good vs. Poor}, grid flashed to the test eye (15 vs. 60 min o f arc squares), eye flashed (dominant vs. n o n d o m i n a n t ) , luminance of the pattern continuously presented to the suppressing eye (0.38 vs. 38.00 mL), square size presented to the suppressing eye (diffuse light, 15, 30 min of arc vs. 60 rain of arc), and the interactions between these effects were statistically evaluated by means of analyses of variance (Bio-Med Program 08V). It should be noted that VEPs were obtained from the flashed or test eye and that the effects of the luminance and of the pattern presented to the suppressing eye were interocular in nature.

Visual evoked potentials and electro-oculograms Monocular evoked potentials to the patterned light flashes were recorded from the surface o f the scalp by means of an active electrode placed 2.5 cm above the inion on the midline and a reference electrode attached to the right earlobe. Redux electrode jelly was rubbed into the skin and applied between the electrode and scalp to reduce skin resistance to less than 10,000 &2. Cortical activity was amplified by a Grass Model 7WC polygraph with 1/2 amplitude high and low frequency filters set at 35 and 1 c/sec respectively and was mo n ito r ed on an oscilloscope for movem e n t and other artifacts. The experiment was temporarily halted when artifacts were apparent. The amplified potentials were averaged

M~ RUSSELL HARTER ET AL. over a 512 msec interval (dwell time 2 msec/ word of m e m o r y ) with a Fabrik-Tek Model 1062 averaging computer. Sampling was initiated 40 msec before stimulus onset in order to obtain prestimulus voltage baselines. A Hewlett-Packard Model 7035B X-Y recorder was used to record the averaged VEPs. Averaged electro-oculograms were obtained under identical conditions in subsequent control runs from surface electrodes placed near the outer canthi of each eye.

Control for attention and experimental procedure Preliminary data indicated that VEPs were influenced by which stimulus was attended and a c c o m m o d a t e d , timt viewed by the left or the right eye, particularly when subjects were anisometropic. To h~sure that this effect would not become c o n f o u n d e d with the experimental conditions, subjects were instructed to always attend, a c c o m m o d a t e , and to give a finger-lift reaction time response to the grid presented to the flashed eye. If the subjects responded t oo slowly (reaction time was longer than their preexperimentally determined mean plus 50 msec), negative feedback was given 500 msec after the light flash in the form of a loud click from a speaker 1 m above the subject's head. Control data were collected to insure that changes in the VEPs could not be attributed to the reaction time response or to eye movements (see Results). The haploscope and response key were located inside an electrically shielded, dimly illuminated (0.20 mL), partially s o u n d p r o o f room, into which white noise was piped for masking purposes. The subjects were repeatedly instructed as to how and when to change the stimulus transparencies viewed by the left and right eyes. T hey were also requested to maintain visual fixation on the crossing of two lines in the center of the continuously illuminated transparency, to keep b o t h eyes correctly aligned in r e s p e c t to the artificial pupils in the haploscope, and to minimize eye and b o d y movementsl

I N T E R O C U L A R S U P P R E S S I O N O F VEPs A N D B I N O C U L A R I T Y

reaction time response to 60 min of arc squares flashed to the test eye. The suppressing eye was continuously presented with either diffuse light or 60 min of arc squares. These data (Fig. 2) were collected to insure that the interocular effects could not be attri-

Results Electrooculogram (EOG) and VEP control data were collected from four of the subjects in each group under conditions where they were instructed to attend, but not give a RESPONSES

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Fig. 2. Visual e v o k e d p o t e n t i a l s ( V E P s ) a n d e l e c t r o o c u l o g r a m s ( E O G s ) t o 6 0 m i n o f arc s q u a r e s flashed t o o n e eye. C o n t r o l d a t a o b t a i n e d w h e n s u b j e c t s d i d n o t give r e a c t i o n times. C o l u m n s r e f l e c t t h e e f f e c t o f w h e t h e r t h e o t h e r eye c o n t i n u o u s l y viewed diffuse light or 6 0 m i n o f arc squares. F o u r s u b j e c t s f r o m G o o d a n d P o o r Bino c u l a r i t y groups. V e r t i c a l solid line 4 0 m s e c a f t e r t r a c e a n d d a s h e d line b e t w e e n 1 5 0 - - 2 5 0 m s e c o n - s e t i n d i c a t e p o i n t in t i m e w h e n r e s p e c t i v e l y t h e flash was p r e s e n t e d a n d V E P a m p l i t u d e was m e a s u r e d ; grid m a r k s o n abscissa i n d i c a t e 1 0 0 msec intervals a f t e r t h e flash.

830 b u t e d to e y e m o v e m e n t s or to the n a t u r e o f the s u b j e c t ' s r e a c t i o n t i m e response. Visual i n s p e c t i o n o f these d a t a i n d i c a t e d t h a t t h e four G o o d and t w o o f the P o o r b i n o c u l a r i t y subjects s h o w e d an overall r e d u c t i o n in VEP a m p l i t u d e w h e n t h e stimulus viewed b y the suppressing eye was c h a n g e d f r o m diffuse light to the 60 m i n o f arc squares. S y s t e m a t i c changes in E O G s w h i c h m i g h t a c c o u n t for this e f f e c t were n o t a p p a r e n t . S u p p r e s s i o n o f VEPs was evident w h e n the subjects d i d n ' t m a k e a R T ( c o n t r o l d a t a ) and w h e n suppression o f R T s was n o t e v i d e n t (see b e l o w ) . T h e r e f o r e , i n t e r o c u l a r s u p p r e s s i o n o f the V E P m a y n o t be a t t r i b u t e d to t h e n a t u r e o f the r e a c t i o n t i m e or the E O G r e s p o n s e . The a m p l i t u d e o f VEPs f r o m individual subjects was q u a n t i f i e d b y first establishing a base line voltage, the average voltage level f r o m 40 m s e c b e f o r e t o 20 m s e c a f t e r the flash, and t h e n m e a s u r i n g the a m p l i t u d e and p o l a r i t y o f the VEP at 3 p o i n t s in t i m e a f t e r the flash in r e f e r e n c e to the base line. T h e s e t h r e e m e a s u r e s were t w o negative c o m p o nents, t h e first b e t w e e n 150 and 200 msec and the second b e t w e e n 200 and 250 m s e c , and a third positive c o m p o n e n t b e t w e e n 250 and 360 msec. It is s o m e w h a t c o n f u s i n g to describe these c o m p o n e n t s in t e r m s o f p e a k s and t r o u g h s since p o l a r i t y m a y invert as a f u n c t i o n o f the e x p e r i m e n t a l c o n d i t i o n s . T h e r e f o r e , m e a s u r e s w e r e t a k e n at fixed latencies. The m e a s u r e selected f o r statistical analyses was the greatest a m p l i t u d e negative d e f l e c t i o n b e t w e e n 150 and 250 m s e c a f t e r the light flash. This m e a s u r e was selected b e c a u s e (1) all subjects had a surface-negative d e f l e c t i o n in this interval; (2) it was the m o s t sensitive in t e r m s o f the e f f e c t s o f t h e experim e n t a l variables and (3) a negative c o m p o n e n t b e t w e e n 150 and 2 0 0 m s e c a f t e r stimulation was f o u n d to be the b e s t m e a s u r e o f sizespecific i n t e r o c u l a r s u p p r e s s i o n b y H a t t e r et al. ( 1 9 7 6 ) . T h e e x a c t latencies at w h i c h this m e a s u r e was t a k e n f o r each s u b j e c t are indic a t e d in T a b l e I and in figures o f V E P s b y a vertical d a s h e d line. Analyses o f variance (biomedical P r o g r a m B M D O 8 V ) w e r e used t o

M~ RUSSELL HARTER ET AL. assess the statistical significance o f changes in this m e a s u r e for b o t h individual subjects and the g r o u p e d d a t a .

Analyses of group data Interocular suppression due to luminance. A l t h o u g h the l u m i n a n c e o f the suppressing e y e in itself did n o t significantly i n f l u e n c e VEPs f r o m the t e s t eye, it did i n t e r a c t with the e f f e c t s of the n a t u r e o f p a t t e r n p r e s e n t e d to b o t h the t e s t and suppressing eyes (Fig. 3). I n t e r o c u t a r s u p p r e s s i o n was g r e a t e r u n d e r the 3 8 . 0 0 m L c o n d i t i o n in t e r m s o f b o t h the e f f e c t o f the stimulus viewed b y the suppressing e y e (P < 0.01) and the i n t e r a c t i o n e f f e c t o f the square size viewed b y b o t h e y e s (P 0.05). The question may be raised as to how accurately individual subjects can be classified as having good or poor binocularity on the basis of interocular suppression of VEPs. If the significance (P < 0.05) o f the mean of the F-ratios reflecting interocular suppression of VEPs for individual subjects (Table I, X F-Ratio) is used as an indicant of good binocular vision, five of the six subjects with good

832

M. RUSSELL HARTER ET AL.

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Fig. 5. Example of VEPs to the 15 min of arc squares from one subject with poor (subject Li, visual acuity of left and right eye 0.8 and 1.0, Z¢~ = 0.2) and good binocularity (subject Ma, visual acuity both eyes 0.9, Z d = 0.7). Arrow indicates flash onset. Four superimposed tracings are two replications from the right (dotted) and left (solid) eyes. Dashed vertical line indicates latency VEP amplitude was measured. Changes in VEPs between rows reflect interocular effects of square size of grids continuously presented to the other eye.

b i n o c u l a r vision, a n d n o n e o f t h e subjects w i t h p o o r b i n o c u l a r vision h a d significant F-ratios. T h e r e f o r e , 11 o u t o f 12 subjects c o u l d be classified c o r r e c t l y on t h e basis o f significant i n t e r o c u l a r s u p p r e s s i o n o f V E P s (P < 0.003). T h e a c c u r a c y o f classification suggests t h a t the magnitude of interocular suppression of VEPs m a y be used t o e s t i m a t e t h e d e g r e e o f s t e r e o a c u i t y or b i n o c u l a r i t y o f e a c h subject. T h e c o r r e l a t i o n b e t w e e n individual s u b j e c t ' s m e a n F-ratio m a g n i t u d e a n d b i n o c u l a r i t y ,

h o w e v e r , o n l y a p p r o a c h e d statistical signific a n c e (r = +0.46, P < 0.07),

Analyses o f reaction time data collected under high luminance conditions T h e p e r c e n t a g e o f t i m e each s u b j e c t r e a c t e d t o t h e flashed s t i m u l u s f a s t e r and slower t h a n t h e i r m e a n r e a c t i o n t i m e w a s c o m p u t e d f o r all the e x p e r i m e n t a l c o n d i t i o n s . Consistent with the VEP data, reaction time was f o u n d t o be i n t e r o c u l a r l y s u p p r e s s e d (was slower) w h e n t h e 38 m L c o n t i n u o u s stimulus

I N T E R O C U L A R SUPPRESSION OF VEPs AND BINOCULARITY

833

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Fig. 6. Changes in VEP amplitude to the 15 and 60 rain of arc squares due to interocular effects of pattern continuously presented to the other eye in individual subjects. Left- and right-hand portions of figures are data from subjects respectively in the control (Good binocularity) and experimental group (Poor binocularity). S/L/R/ZD indicates subject/visual acuity of left eye/visual acuity of right eye/standard depth perception score (see Table I and text).

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was changed from diffuse light to the grid patterns (P < 0.01, Fig. 7). Changes in RT, associated with size-specific interocular effects and group differences, did not approach statistical significance.

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Discussion

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m

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CONTINUOUS GRID TO OTHER EYE (38 mL) (min of orc)

Fig. 7. Effects of the stimulus continuously viewed by one eye on the reaction time to the stimulus flashed to the other eye. The continuous stimulus was 38 mL. Reaction time (RT) is expressed as the percentage of responses faster than the mean RT for each subject at the beginning of this experiment. Data have been averaged across subjects, binocularity groups, replications, eyes, and square size to the flashed eye.

The results support the hypothesis o f sizespecific interocular suppression of VEPs; continuous presentation of a given grid size to one eye resulted in reduced VEP amplitude to that same grid size flashed to the other eye. The a m o u n t of interocular suppression decreased as the grid sizes presented to the two eyes become progressively more discrepant. This corroborates previous findings based on both VEP (Hatter et al. 1976) and psychophysical (Maudarbocus and Ruddock 1973)

834 measures. A second type of interocular suppression, due to the nature of pattern per se, was also noted which is similar to that reported by Harter et al. {1974). The size-specific suppression was most evident when the intensity of the suppressing pattern was high (38.00 mL). A similar effect has been reported on psychophysically measured spatial frequency adaptation when both the test and adapting stimuli were presented intraocularly (Bagrash 1973). The present data indicate that the low intensity of the suppressing stimulus {0.40 mL) used by Harter et al. (1974) may account for the lack of size-specific interocular suppression of VEPs in their study. Both pattern and pattern-specific interocular suppression were more evident in subjects with good as compared to poor binocularity, particularly in VEPs to the 15 rain of arc squares. Eleven of the twelve subjects could be classified post hoc correctly as having good or poor binocularity on the basis of significant interocular suppression of the VEP. This finding corroborates previous psychophysical data which indiate the interocular transfer of the tilt-aftereffect is dependent on the binocularity of the subjects (Movshon et al. 1972; Mitchell and Ware 1974). Given these findings, why was the magnitude of the interocular suppression of VEPs (as measured by F-ratios obtained from the analyses of variance) only moderately correlated with the degree of binocularity? Mitchell and Ware (1974) reported a much higher correlation, possibly because they employed the following conditions: they used a more accurate measure of stereoacuity; they controlled for intraocular effects, such as refractive error and visual acuity, by expressing interocular transfer in terms of the percentage of the intraocular effect; they used a smaller grid size {higher spatial frequency) which, according to the present study, should enhance the relationship between interocular transfer and binocularity; and they used a more heterogenous sample of subjects in terms of stereoacuity.

M. RUSSELL HARTER ET AL. The relationship between binocularity and size-specific interocular suppression of VEPs may be attributed to a number of factors. Subjects with poor binocularity tended to have greater lateral phorias {Table I) and may have had difficulty maintaining single binocular vision. Although subjects were instructed to halt stimulation when the suppressing and test stimuli fell on noncorresponding retinal areas, the Poor bim)cularity subjects may not have followed these instructions. This was unlikely, however, since the correlation between phorias and interocular suppression of VEPs did not approach statistical significance and since both groups reflected the same degree of interocular suppression of behavioral RT due to pattern per se. Another possibility is that subjects with poor binocularity also had poor visual acuity and, thus, could not discriminate the suppressing stimuli. This also is unlikely since all subjects had visual acuities better than 20/29 (except for 20/67 in De's right eye) and discriminated the stimuli both psychophysically and electrophysiologically. The data from individual subjects also indicate some subjects with poor binocularity had 20/20 or better visual acuity (Sa and Ge) but still did not show statistically si~lificant size-specific interocular suppression of VEPs. The moderate degree of relationship between stereoacuity and interocular suppression of VEPs may be attributed to the possbility that these two factors are mediated by different physiological mechanisms but that both mechanisms require binocular convergence on central neurons. For example, the former could be related to disparities in the aligment of the monocular receptive fields of binocular neurons; whereas, the latter could be related to the size of the receptive fields of the binocular neurons (as discussed below). Both of these mechanisms require binocular convergence. It may be noted that VEPs have been obtained to transient changes in retinal disparity (Fiorentini and Maffei 1970; Regan and Spekreijse 1970) which suggest a direct measure of stereopsis.

INTEROCULAR SUPPRESSION OF VEPs AND BINOCULARITY The present data also suggest another type of interdependence. Binocularity appeared to be more associated with mechanisms processing high spatial frequencies or small square sizes. Only subjects with good binocularity reflected size-specific interocular suppression of VEPs to the small square (15 min of arc); whereas Poor binocularity subjects reflected some degree of size-specific interocular suppression of VEPs to the 60 min o f arc grid. In conclusion, size-specific interocular suppression of VEPs, and the influence of binocularity and stimulus intensity on this suppression, may be attributed to the nature of binocular receptive fields of cortical neurons. Animals studies indicate cortical neurons have binocular receptive fields organized in a manner so as to maximize sensitivity to patterns of a specific size and orientation when presented to approximately corresponding retinal areas (Hubel and Wiesel 1962; Barlow et al. 1967; Pettigrew et al. 1968; Bishop et al. 1971; Minke and Auerback 1972). Harter et al. (1976) proposed that saturation of binocular neurons by inputs from one eye (the continuously stimulated or suppressing eye) would occlude or prevent any additional response of these neurons to inputs from the other eye (the flashed eye), assuming such neurons exist in the human visual system. The VEPs to the flashed eye would, thus, be suppressed. Within the context of this model, the interocular suppression of VEPs in the present study indicates (a) greater binocular convergence on cortical neurons in subjects with good as compared to poor binocularity; (b) greater binocular convergence on cortical neurons when both eyes view identical as compared to different grid sizes; and (c) greater saturation of the binocular cortical neurons when the suppressing stimulus was high as compared to low in intensity.

Summary Evoked cortical potentials (VEPs) to grid patterns flashed to one eye were suppressed

835

in amplitude when grid patterns were continuously presented to the other eye. The degree of interocular suppression of VEPs was influenced by the stereoacuity of the subjects. VEPs were obtained to each of two grid sizes flashed to one eye (individual squares subtending 15 and 60 min of arc) and changes in amplitude of these VEPs were considered as a function of four stimuli continuously presented to the other eye (diffuse light, 15, 30, and 60 min of arc squares in grids). Interocular suppression of VEPs was greater (a) when the continuously presented grid was of high (38.00 mL) as compared to low (00.38 mL) intensity, (b) when the continuous and flashed grids were of the same as compared to different sizes, and (c) in six subjects who had good as compared to six subjects who had poor binocularity. Eleven of the twelve subjects could be classified correctly as having good or poor binocularity on the basis of statistically significant interocular suppression of VEPs. The results were interpreted in terms of centrally located binocular neurons responsive to specific grid sizes or spatial frequencies and the decreased functioning of such neurons in subjects with poor binocularity.

Rdsumd Vision binoculaire chez l'homme: suppression interoculaire des potentiels dvoquds visuels spdcifiques de la dimension Les potentiels ~voqu~s corticaux (VEPs) des patterns en damier dclair~s devant un oeil subissant une suppression d'amplitude quand les patterns sont prdsentds de fa~on continue l'autre oeil. Le degr~ de suppression interoculaire des VEPs est influencd par la st~rdoacuit~ des sujets. Les VEPs sont obtenus pour chacune des deux tailles de damier dclair~s devant un oeil (chaque carr~ soustendant 15' et 60'; les modifications d'amplitude de ces VEPs sont consid~r~es comme une fonction des 4 stimuli pr~sent~s de faqon continue l'autre oeil (lumi~re diffuse, damiers de carrds

836

de 15', 30' et 60')). La suppression interoculaire des VEPs est plus grande (a) quand le damier pr~senge de fa~on continue est d'une intensit~ ~lev~e (38,00 mL) que lorsqu'il est de faible intensit~ {00.38 mL), (b) quand les damiers continus ~clair~s sont de la m~me taille que lorsqu'ils sont de tailles diff~rentes et (c) chez ces 6 sujets qui ont une bonne binocularit~ que chez ces 6 sujets qui ont une mauvaise binocularitY. Onze des douze sujets pouvaient ~tre classes correctement comme ayant une bonne ou mauvaise binocularit~ sur la base d'une suppression interoculaire des VEPs statistiquement significative. Ces r~sultats sont interpr~t~s en terme de neurones binoculaires de localisation centrale r~actifs des tailles de damiers sp~cifiques ou ~ des fr~quences spatiales et de fonctionnement diminu~ de ces neurones chez des sujets avec mauvaise binocularitY. References Abadi, R.V. Induction masking -- A study of some inhibitory interactions during dichoptic viewing. Vision Res., 1976, 16: 269--275. Bagrash, F.M. Size-selective adaptation: Psychophysical evidence for size-tuning and the effects of stimulus contour and adapting flux. Vision Res., 1973, 1 3 : 5 7 5 598. Barlow, H.B., Btakemore, C. and Pettigrew, J.D. The neural mechanism of binocular depth discrimination. J. Physiol. (Lond.), 1967, 193: 327--342. Bishop, P.O., Henry, G.H. and Smith, C.J. Binocular interaction fields of single units in the cat striate cortex. J. Physiol. (Lond.), 1971, 216: 39--68. Blakemore, C. and Campbell, F.W. On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. J. Physiol. (Lond.), 1969, 203: 237--260. Blakemore, C., Muncey, J.P.J. and Ridley, R.M. Stimulus specificity in the human visual system. Vision Res., 1973, 13: 1915--1931. Campbell, F.W. and Maffei, L. Electrophysiological evidence for the existence of orientation and size detectors in the human visual system. J. Physiol. (Lond.), 1970, 207: 635--652. Fiorentini, A. and Maffei, L. Electrophysiological evidence for binocular disparity detectors in human visual system. Science, 1970, 169: 208--209. Harter, M.R., Seiple, W.H., and Musso, M. Binocular summation and suppression: visually evoked corti-

M. RUSSELL HARTER ET AL. cal responses to dichoptically presented patterns of different spatial frequencies. Vision Res., 1974, 14: 1169--1180. Harter, M.R., Towle, V.L. and Muss(), M.F. Size specificity and inter-ocular suppression: Monoculm evoked potentials and reaction times. Vision Res., 1976, 16: 1111--1117. ilubel, D.H. and Wiesel, T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. ,1. Physiol. (Lond.), 1962, 160: 106--154. tiubel, D. and Wiesei, T Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol., 1965, 28: 1041--1059. Maffei, L., Fiorentini, A. and Bisti, S. Neural correlate of perceptual adaptation to gratings. Science, 1973, 182: 1036--1038. Maudarbocus, A.Y. and Ruddock, K.H. The influence of wavelength on visual adaptation to spatial periodic stimuli. Vision Res., 1973, 13: 993--998. Mecacci, L. and Spineili, D. The effects of spatial frequency adaptation on human evoked potentials. Vision Res., 1976, 16: 477--479. Minke, B. and Auerbach, E. Latencies and correlation ill single units and visual evoked potentials in the cat striate cortex following monocular and binocular stimulations. Exp. Brain Res., 1972, 14: 409-422. Mitchell, D.E. and Wal'e, C. Interocular transfer of a visual aftereffect in normal and stereoblind humans. J. Physiol. (Lond.), 1974, 236: 707--721. Movshon, J.A., Chambers, B.E.I. and Blakemore, C. Interocular transfer in normal humans and those who lack stereopsis. Perception, 1972, 1 : 4 8 3 :190. Musso, M.F. and Harter, M.R. Visually evoked p o ~ rials and selective masking with patterned flashes of different spatial frequencies. Vision Res., 1975, 15: 23]--238. Pettigrew, J.D., Nikara, T. and Bishop, P.O. Binocular interaction on single units in cat striate cortex: Simultaneous stimulation with single moving slits with receptive fields in correspondence. Exp. Brain Res., 1968, 6: 391- 410. Regan, D. and Spekreijse, H. Electrophysiological correlate of binocular depth perception in man. Nature (Lond.), 1970~ 225: 92--94. Spekreijse, H., Khoe, L.H. and van der Tweel, L.H. A case of amblyopia; electrophysiology and psych()physics of luminance and contrast. In G.B. Arden (Ed.), The Visual System; Neurophysiology, Biophysics, and their Clinical Applications. Plenum Press, New York, 1 9 7 2 : 1 4 1 --156. Weisel, T.N. and Hubel, D.H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol., 1965, 28: 1029--1040.