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Grating and flicker sensitivity in the near and far periphery: Naso-temporal asymmetries and binocular summation
Vision Res. Vol. 34, No. 21, pp. 2841-2848, 1994
Pergamon
0042-6989(94)E0084-X
Copyright © 1994 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0042-6989]94 $7.00 + 0.00
Grating and Flicker Sensitivity in the Near and Far Periphery: Naso-Temporal Asymmetries and Binocular Summation SCOTT S. GRIGSBY,* BRIAN H. TSOUt Received 16 December 1993, in revised form 17 March 1994
A variety of recent physiological and psychophysical experiments provide evidence for a large asymmetry between nasal and temporal processing outside of the central 40o of visual field. Binocular processing has also been found to be reduced outside of this region even though the individual left and right eye fields continue to overlap for a full 120 °. In an effort to help quantify these findings, monocular and binocular grating and flicker contrast sensitivities were measured in the fovea and in the near and far periphery. The results show a large asymmetry between nasal and temporal retinal grating sensitivity in the far periphery especially at high spatial frequencies. A smaller asymmetry was found for flicker but no differential effect of flicker frequency was found. The summation results are consistent with previous findings in showing greatly reduced binocular processing outside of the central 40°; this is especially true for the grating stimuli. These results are discussed with respect to possible physiological mechanisms. Peripheral vision Binocularsummation Contrast sensitivity Naso-temporal asymmetry
INTRODUCTION The spatial density of photoreceptors measured in the far periphery of whole-mount human retinae is asymmetrical for the nasal and temporal hemi-retinae (Curcio, Sloan, Kalina & Hendrickson, 1990). At equivalent eccentricities beyond 20 deg, rod and cone density is ~40-50% higher in nasal retina than in temporal retina. A larger asymmetry is found for the spatial distribution of ganglion cells. Retinal ganglion cell density in the far periphery is more than 300% higher in nasal retina than temporal retina (Curcio & Allen, 1990). No asymmetry is found within the central 40 deg. Spillmann, Ransom-Hogg and Oehler (1987) have shown that there is a similar naso-temporal asymmetry in the diameters of the receptive fields of monkey ganglion cells and the perceptive fields of human observers. This naso-temporal retinal asymmetry may have a correlate in visual cortex. In macaque monkeys, the portion of area V1 of visual cortex corresponding to the far periphery is found to have ocular dominance stripes for the contralateral eye (nasal retina) that are wider than those for the ipsilateral eye (temporal retina) (Le Vay, Connolly, Houde & van Essen, 1985). In some portions of cortex the striped structure actually breaks *Logicon Technical Services, Inc., P.O. Box 317258, Dayton, OH 45431-7258, U.S.A. [Email [email protected]]. tArmstrong Laboratory, AL/CFHV, Wright-Patterson AFB, OH 45433-7022, U.S.A. [Email btsou(~falcon.aamrl.wpafb.af.mil].
down so that small areas of ipsilateral input are completely surrounded by large areas of contralateral input. This structure implies an asymmetry in retinal input to cortex in which nasal input dominates over temporal and, as with the human retinal cell data above, the asymmetry occurs only for areas corresponding to visual field outside of the central 40 deg. Psychophysical measurements show that these anatomical asymmetries of nasal and temporal retinal and cortical processing in the far periphery affect threshold and suprathreshold sensitivity. Far peripheral nasal retina has been found to have a higher sensitivity than temporal retina for chromatic and achromatic resolution targets, vernier acuity, and luminance and chromatic discrimination (Anderson, Mullen & Hess, 1991; Fahle & Schmid, 1988; Stabell & Stabell, 1982; Noorlander, Koenderink, den Ouden & Edens, 1983). This asymmetry may also be responsible for a breakdown in binocular processing in the far periphery. Perimetric measurements show that under optimal conditions the human achromatic visual field extends approx. 200 deg horizontally by 130 deg vertically. Of this 200 deg wide area, approx. 120 deg can be seen by both eyes at the same time. However, psychophysical measurements show that there is appreciable binocular processing only within the central 40 deg of visual field. For example, in a study of depth perception, Richards and Regan (1973) measured the extent of the stereoscopic field for a target sinusoidally modulated in
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SCOTT S. GR1GSBY and BRIAN H. TSOU
disparity (see also Regan, Collewijn & Erkelens, 1986). No depth was seen at eccentricities > ~ 20 deg along the horizontal meridian. Fahle (1987) has shown a more direct correspondence between the naso-temporal asymmetry and binocular inhibition. Two distinct stimuli were presented dichoptically at corresponding points along the horizontal meridian so that the stimuli elicited rivalry. Neither stimulus dominated the inhibition in the central 40deg of visual field. However, when stimuli were presented at eccentricities > 20deg the stimulus presented to the nasal hemi-retina was seen more than twice as much as that presented to the temporal hemi-retina. Finally, binocular summation is also reduced outside of the central 40deg. Wood, Collins and Carkeet (1992) showed that binocular summation of small perimetric targets (Goldmann equivalents I, III and V) is greatly reduced in the far periphery. However, target size had an influence on the extent of summation and its rate of change with eccentricity. Binocular summation of the smallest stimuli (target I, 0.108deg) dropped fairly rapidly while that of the largest stimuli (target V, 1.724deg) stayed nearly constant. Furthermore, for the smaller targets (I and III), the amount of summation was found to be correlated with the difference between the nasal and temporal sensitivity in that larger naso-temporal differences led to smaller summation ratios. This relationship was not found for the larger target. These results imply that the amount of naso-temporal asymmetry and the extent of the binocular field may be dependent on the stimulus parameters. The purpose of the following experiment is to provide systematic measurements of monocular and binocular grating and flicker contrast sensitivity in the near and far periphery. Any effects of spatial or temporal frequency on the naso-temporal asymmetry or on binocular summation will be discussed with respect to the underlying physiology. METHODS
Photopic contrast sensitivities for sinusoidal gratings and flicker were measured as a function of horizontal eccentricity, thresholds were measured at nine eccentricities (0, _+4, _+8, + 24, _+32 deg) for both the right and left eyes and binocularly. The stimuli were generated using the VisionWorks computer graphics display system (VRG, Inc., Durham, N.H.). This system uses a PC computer and a TI 34020 graphic controller with ! 5 bits of gray-scale. The images are presented on a high resolution (1024 x 512 pixels) monitor with a 120 Hz refresh rate. The monitor was photometrically linearized and calibrated for stimulus contrast. Both the grating and flicker stimuli were generated full screen but were placed in a two-dimensional Gaussian spatial window with a = 1.5 deg. The grating stimuli were oriented vertically and were presented in a rectangular temporal envelope for 0.5 sec. The spatial fre-
quency ranged from 0.4 to 16.0 c/deg. The flicker stimuli were presented for 1.0 sec in a raised cosine temporal envelope. The flicker frequency ranged from 1.0 to 40.0 Hz. The stimuli had a mean luminance equal to that of the blank background (55 cd/m2). A screen, on which small fixation points were placed, surrounded the monitor and had the appropriate curvature to keep the observer's accommodation constant. The screen was luminance matched to the monitor, however, a small amount of chromatic mismatch was still evident. Observers used a chinrest and were instructed to fixate the appropriate point. Fixation was not monitored; however, the observers, although naive to the purpose of this experiment, were experienced at doing psychophysical experiments and at maintaining fixation for peripheral measurements. The observers had natural pupils and, for the monocular conditions, the unused eye was covered with a semi-translucent patch. Thresholds were measured using a modified Q U E S T procedure (the " Z E S T " procedure; see King-Smith, Grigsby, Vingrys, Benes & Supowit, 1994). The ZEST procedure uses a likelihood function to estimate thresholds with a yes-no staircase paradigm. Twentyfive cycles were run for each stimulus. The mean of the final probability distribution was used as an estimate of the threshold. Stimulus presentations were preceded by 0.5 sec by a warning tone. Observers were instructed to respond "yes" only to the percept of a grating (for the grating experiments) or flicker (for the flicker experiments). Repeated measures analysis of variance were done on the data. Individual contrasts were determined using t-tests. Eleven observers (10 males, 1 female; age range, 19 30yr; mean, 23.8yr) were used for the measurements. All had uncorrected Snellen acuities of 20/20 or better and normal visual fields as determined by standard Humphrey perimetery. Each observer ran a total of six 2 hr sessions (with numerous breaks) plus a I hr training session over a period of 2 weeks. Conditions were randomized between observers and days. Informed consent was obtained from all observers. RESULTS Figure 1 shows the contrast sensitivities for the grating and flicker stimuli averaged across all eleven observers. Preliminary analysis indicated no significant differences between the results for the left and right eyes or left and right fields, therefore the nasal and temporal data are an average of the two eyes. In the near periphery (4 and 8deg), binocular sensitivity is appreciably greater than nasal and temporal sensitivity--which are roughly equivalent--for both flicker and gratings. In the far periphery (24 and 32 deg), temporal retinal sensitivity for flicker has decreased slightly compared to nasal sensitivity but binocular sensitivity is still appreciably greater than either. However, temporal retinal sensitivity for gratings has dropped significantly below nasal sensitivity and binocular sensitivity is now effectively the same
C O N T R A S T SENSITIVITY IN T H E P E R I P H E R Y
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F I G U R E 1, Monocular and binocular grating and flicker contrast sensitivities in the fovea and at four peripheral eccentricities.
as nasal sensitivity alone. These findings are further analyzed below. In Fig. 2(a), the logarithm of the ratio of the nasal to temporal retinal sensitivity is plotted as a function of eccentricity and spatial frequency. The corresponding plot for flicker frequency is shown in Fig. 2(b). Pairwise comparisons were done for all of the data points. Significant differences (P ~< 0.05) between nasal and
temporal sensitivities are shown as solid circles. Open circles indicate no statistically significant difference at the 0.05 level. Table 1 shows the A N O V A results comparing nasal and temporal retinal sensitivity for (a) gratings and (b) flicker. N o significant differences were found between nasal and temporal sensitivity at 4 deg for gratings or flicker ( P / > 0.2660). A significant difference (P = 0.0408)
2844
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CONTRAST SENSITIVITY IN THE PERIPHERY
2845
TABLE 1. Analysis of variance results for nasal vs temporal sensitivity for gratings and flicker Eccentricity
Nasal vs temporal sensitivity
Mean A*
Interaction w/frequency
(a) Gratings
4deg 8 deg 24deg 32 deg
F(I, F(I, F(I, F(I,
10)= 1.39 10) = 5.07 10) = 64.78 10) = 37.39
P P P P
=0.2660 = 0.0408 = 0.0001 = 0.0001
0.037 0.041 0.344 0.449
F(7, 70) = 0.16 F(6, 60) = 0.92 F(4, 40) = 9.64 F(3, 30) = 26.22
P P P P
=0.9914 = 0.4858 = 0.0001 = 0.0001
F(I, F(I, F(1, F(1,
10) = 0.07 10)= 1.96 10) = 36.57 10) = 28.23
P P P P
= 0.7995 =0.1921 = 0.0001 = 0.0003
0.005 0.023 0.120 0.185
F(7, F(7, F(7, F(7,
P P P P
= 0.7468 =0.1504 = 0.5600 = 0.2352
(b) Flicker
4 deg 8deg 24 deg 32 deg
70) = 0.61 70) = 1.60 70) = 0.84 70) = 1.36
*Mean A is the difference in log units between nasal and temporal retinal sensitivity.
was found at 8 deg for gratings but this difference was very small (mean difference across frequencies = 0.041 log units). No significant difference was found between nasal and temporal sensitivity at 8 deg for flicker (P =0.1921). At 24 and 32deg, nasal sensitivity was found to be significantly greater than temporal sensitivity for both gratings and flicker (P ~< 0.0003). Table 1 also shows that this sensitivity difference in the far periphery has an interaction with spatial frequency (P ~< 0.0001) in that the naso-temporal difference increased with increasing spatial frequency. There was no significant differential effect of flicker frequency (P ~> 0.2352). Figure 3(a,b) shows the binocular summation ratios (binocular/nasal sensitivity) as a function of eccentricity and frequency for gratings and flicker, respectively. Table 2 shows the A N O V A results for the binocular summation comparisons (binocular vs nasal sensitivity) for (a) gratings and (b) flicker in the near and far periphery. Significant binocular summation (P ~ 0.0001) was found in the near periphery (4 and 8 deg) for both grating and flicker stimuli. There was no significant interaction with frequency for grating stimuli (P ~> 0.2164) but the flicker stimuli did show an interaction (P = 0.0032) at 4 deg eccentricity. The interaction is due to a slightly reduced amount of summation at the highest flicker frequencies (24 and 40 Hz) and does not appear to be a major effect. For gratings in the far periphery, a significant (P = 0.0263) but reduced amount of summation was found at 24 deg eccentricity but no significant summation was found at 32 deg (P = 0.2355). Significant levels (P ~< 0.0036) of summation were found at both 24 and 32 deg for flicker. There was no effect of spatial or flicker frequency on binocular summation in the far periphery (P >/0.2722). The relationship between the extent of the n a s o temporal asymmetry and the amount of binocular summation can be seen in Fig. 4. Regression lines have been fit through the data for gratings and flicker (R 2 = 0.507, s l o p e = - - 0 . 4 1 9 for gratings and R 2 = 0 . 6 7 4 , slope = - 0 . 7 9 2 for flicker). The plot shows that for both flicker and gratings the amount of summation decreases as the naso-temporal sensitivity differences increases and the amount of summation is effectively zero when the
sensitivity difference is > ~ 2 : 1 . However, the relationship is fairly irregular and there is a large range of summation ratios even when nasal and temporal retinal sensitivities are similar. DISCUSSION The results are consistent with previous studies in showing a large asymmetry between nasal and temporal retinal sensitivity beyond 20 deg eccentricity. However, the asymmetry seems to be larger for gratings than flicker and shows an effect of spatial but not flicker frequency. There are at least three possible causes for the spatial frequency dependent difference of nasal and temporal retinal sensitivity in the far periphery: (1) the difference in photoreceptor cell density (Curcio et al., 1990), (2) the difference in ganglion cell density (Curcio & Allen, 1990), or (3) the difference in ganglion cell receptive field size (Spillmann et al., 1987) between the two hemi-retinae. Anderson et al. (1991) have shown that the limit of spatial resolution in the periphery is most likely due to ganglion cell density and not receptor density or optical factors. The Nyquist frequency limit of the ganglion cell mosaic as a function of eccentricity is qua.litatively similar to the drop in resolution. Also, when ganglion cell spatial acuity is compared with the Nyquist limits for individual ganglion cells as a function of eccentricity, spatial acuity exceeds the cell Nyquist limit at eccentricities beyond 15 deg. This, Anderson et al. suggest, means that the limit to resolution in the periphery is due to the sampling density of the ganglion cells and not the individual cell receptive field size. Therefore, the asymmetry they find in spatial resolution between the temporal and nasal hemi-retinae is simply a reflection of the asymmetry between the ganglion cell densities. The above findings suggest that it is the ganglion cell density and not ganglion cell receptive field size or photoreceptor density that is the predominant factor in limiting spatial resolution in the far periphery. This can be used to account for the asymmetry in the nasal and temporal retinal contrast sensitivity measurements found here. Virsu and R o v a m o (1979) have shown that the shape of the contrast sensitivity curve is related to the
2846
SCOTT S. G R I G S B Y and B R I A N H. TSOU
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CONTRAST
2847
SENSITIVITY IN THE PERIPHERY
T A B L E 2. A n a l y s i s of v a r i a n c e results for b i n o c u l a r vs nasal sensitivity for gratings a n d flicker Eccentricity
Binocular summation
M e a n A*
I n t e r a c t i o n w/frequency
(a) Gratings 4 8 24 32
deg deg deg deg
F(1, F(1, F(I, F(1,
10) 10) 10) 10)
= = = =
77.61 234.90 6.78 1.59
P P P P
= = = =
0.0001 0.0001 0.0263 0.2355
0.209 0.177 0.083 0.045
F(7, F(6, F(5, F(4,
70) 60) 50) 40)
= = = =
1.41 0.80 0.32 0.48
P P P P
= = = =
0.2164 0.5740 0.8973 0.7484
F(I, F(I, F(1, F(1,
10) 10) 10) 10)
= = = =
130.71 109.59 54.81 14.23
P P P P
= = = =
0.0001 0.0001 0.0001 0.0036
0.245 0.212 0.157 0.091
F(7, F(7, F(7, F(7,
70) 70) 70) 70)
= = = =
3.44 2.12 1.28 0.98
P P P P
= = = =
0.0032 0.0522 0.2722 0.4499
(b) Flicker 4 8 24 32
deg deg deg deg
* M e a n A is the difference in log units between b i n o c u l a r and nasal retinal sensitivity.
far temporal hemi-retina as compared to the nasal hemi-retina due to the reduced ganglion cell density. Differences in ganglion cell density should not affect the shape of the flicker sensitivity curve in that density alone would not be expected to affect the temporal processing characteristics of the individual ganglion cells. However, different amounts of pooling of ganglion cell signals could lead to differences in maximal sensitivity (unless the signals are somehow renormalized), i.e. less pooling would mean a lower signal/noise ratio and therefore an overall frequency-nonspecific decrease in sensitivity such as that found here. The summation data are also consistent with other studies in finding reduced binocular processing in the far periphery. Figure 5 shows that the average amount of binocular summation across all spatial frequencies drops off rapidly in the periphery and is near zero by 24 deg eccentricity. Average flicker summation shows a less rapid drop off but it too is significantly reduced by 32 deg eccentricity. As shown in Fig. 4, this loss of binocular summation in the far periphery is correlated
ganglion cell receptive field spacing; increased receptive field spacing leads to a decreased maximal sensitivity, a lower peak frequency and a lower high-frequency cutoff. These are the same effects found in the grating sensitivity plots of Fig. 1 for 24 and 32 deg eccentricity; contrast sensitivity for the temporal hemi-retina shows a reduction in the maximal sensitivity, the peak frequency, and the cut-off frequency as compared to the nasal hemi-retina. This implies that the shape of the contrast sensitivity curves are a reflection of the underlying ganglion cell density, and it is this difference in the shape of the contrast sensitivity curves which leads to the spatial frequency dependency of the nasa-temporal asymmetry. Ganglion cell density may also explain the frequency independence of the nasa-temporal asymmetry for flicker. Temporal retinal sensitivity is reduced compared to nasal sensitivity for all flicker frequencies by approximately the same amount. This can be seen in the flicker results of Fig. 1 for 24 and 32 deg eccentricity. This could simply be attributed to a reduced signal strength for the 0.4
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Log(Nasal/Temporal) F I G U R E 4. Scatter p l o t s h o w i n g the r e l a t i o n s h i p between the a m o u n t o f b i n o c u l a r s u m m a t i o n a n d the a m o u n t o f n a s a - t e m p o r a l a s y m m e t r y . R e g r e s s i o n lines are s h o w n i n d i v i d u a l l y for the g r a t i n g a n d flicker d a t a (R 2 = 0.507, slope = - 0 . 4 1 9 for g r a t i n g s a n d R 2 = 0.674, slope = - 0 . 7 9 2 for flicker).
2848
SCOTT S. GRIGSBY and BRIAN H. TSOU
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with the extent of the naso-temporal sensitivity asymmetry for both flicker and gratings. While a correlation does not imply a cause-and-effect relationship, the results suggest that binocular processing drops off because nasal sensitivity starts to dominate over temporal sensitivity and, therefore, the signals are no longer useful for binocular processing. Another possible physiological correlate for the lack of binocular processing especially for spatial stimuli may be found in the topographic organization of the parvocellular layers of the lateral geniculate nucleus (LGN). Connolly and van Essen (1984), using data of their own and that of Malpeli and Baker (1975), constructed two-dimensional topographic maps of the separate layers of the LGN of macaque monkey. The two magnocellular layers (LGN layers 1 and 2) as well as parvocellular layers 3 and 6 have visual field representations extending out to ~80 deg eccentricity and beyond. However, the field representations for parvocellular layers 4 and 5 do not extend much beyond 20 deg eccentricity. Because both the extent of the binocular field-of-view; as evidenced by the summation, stereo and rivalry data, and the extent of the topographic boundaries of layers 4 and 5 correspond only to the central 40 deg of visual field, the hypothesis can be made that parvocellular layers 4 and 5 have a large role in relaying binocular information to cortex. REFERENCES Anderson, S. J., Mullen, K. T. & Hess, R. F. (1991). Human peripheral spatial resolution for achromatic and chromatic stimuli: Limits imposed by optical and retinal factors. Journal of Physiology, 442, 47~64. Connolly, M. & van Essen, D. (1984). The representation of the visual field in parvicellular and magnocellular layers of the lateral geniculate nucleus in the Macaque monkey. Journal of Comparative Neurology, 226, 544-564. Curcio, C. A. & Allen, K. A. (1990). Topography of ganglion cells in the human retina. Journal o[" Comparative Neurology, 300, 5-25.
Curcio, C. A., SIoan, K. R., Kalina, R. E. & Hendrickson, A. E. (1990). Human photoreceptor topography. Journal of Comparative Neurology, 292, 497 523. FaMe, M. (1987). Naso-temporal asymmetry of binocular inhibition. Investigative Ophthalmology & Visual Science, 28, 1016-1017. Fahle, M. & Schmid, M. (1988). Naso-temporal asymmetry of visual perception and of the visual cortex. Vision Research, 28, 293 300. King-Smith, P. E., Grigsby, S. S., Vingrys, A. J., Benes, S. C. & Supowit, A. (1994). Efficient and unbiased modifications of the QUEST threshold method: Theory, simulations, experimental evaluation and practical implementation. Vision Research, 34, 885 912. LeVay, S., Connolly, M., Houde, J. & van Essen, D. C. (1985). The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. Journal of Neuroscience, 5, 486-50 I. Malpeli, J. G. & Baker, F. H. (1975). The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta. Journal of Comparative Neurology, 161, 569 594. Noorlander, C., Koenderink, J. J., den Ouden, R. J. & Edens, B. W. (1983). Sensitivity to spatiochromatic colour contrast in the peripheral visual field. Vision Research, 23, 1 11. Regan, D., Collewijn, H. & Erkelens, C. (1986). Necessary conditions for motion in depth perception. Investigative Ophthalmology and Visual Science, 27, 584-597. Richards, W. & Regan, D. (1973). A stereo field map with implications for disparity processing. Investigative Ophthalmology, 12, 904 909. Spillmann, L., Ransom-Hogg, A. & Oehler, R. (1987). A comparison of receptive and perceptive fields in man and monkey. Human Neurobiology, 6, 51 62. Stabell, U. & Stabell, B. (1982). Color vision in the peripheral retina under photopic conditions. Vision Research, 22, 839 844. Virsu, V. & Rovamo, J. (1979). Visual resolution, contrast sensitivity, and the cortical magnification factor. Experimental Brain Research, 3Z 475 494. Wood, J. M., Collins, M. J. & Carkeet, A. 0992). Regional variations in binocular summation across the visual field. Ophthalmic and Physiological Optics, 12, 46 51.
Acknowledgements
This work was supported by AF workunit 71841158 of Armstrong Laboratory (Wright-Patterson Air Force Base, Ohio). The authors would like to thank Beth Rogers-Adams and Chuck Goodyear of Logicon Technical Services, Inc (Dayton, Ohio) for their assistance on this study.
Pergamon
0042-6989(94)E0084-X
Copyright © 1994 Elsevier Science Ltd Printed in Great Britain. All rights reserved 0042-6989]94 $7.00 + 0.00
Grating and Flicker Sensitivity in the Near and Far Periphery: Naso-Temporal Asymmetries and Binocular Summation SCOTT S. GRIGSBY,* BRIAN H. TSOUt Received 16 December 1993, in revised form 17 March 1994
A variety of recent physiological and psychophysical experiments provide evidence for a large asymmetry between nasal and temporal processing outside of the central 40o of visual field. Binocular processing has also been found to be reduced outside of this region even though the individual left and right eye fields continue to overlap for a full 120 °. In an effort to help quantify these findings, monocular and binocular grating and flicker contrast sensitivities were measured in the fovea and in the near and far periphery. The results show a large asymmetry between nasal and temporal retinal grating sensitivity in the far periphery especially at high spatial frequencies. A smaller asymmetry was found for flicker but no differential effect of flicker frequency was found. The summation results are consistent with previous findings in showing greatly reduced binocular processing outside of the central 40°; this is especially true for the grating stimuli. These results are discussed with respect to possible physiological mechanisms. Peripheral vision Binocularsummation Contrast sensitivity Naso-temporal asymmetry
INTRODUCTION The spatial density of photoreceptors measured in the far periphery of whole-mount human retinae is asymmetrical for the nasal and temporal hemi-retinae (Curcio, Sloan, Kalina & Hendrickson, 1990). At equivalent eccentricities beyond 20 deg, rod and cone density is ~40-50% higher in nasal retina than in temporal retina. A larger asymmetry is found for the spatial distribution of ganglion cells. Retinal ganglion cell density in the far periphery is more than 300% higher in nasal retina than temporal retina (Curcio & Allen, 1990). No asymmetry is found within the central 40 deg. Spillmann, Ransom-Hogg and Oehler (1987) have shown that there is a similar naso-temporal asymmetry in the diameters of the receptive fields of monkey ganglion cells and the perceptive fields of human observers. This naso-temporal retinal asymmetry may have a correlate in visual cortex. In macaque monkeys, the portion of area V1 of visual cortex corresponding to the far periphery is found to have ocular dominance stripes for the contralateral eye (nasal retina) that are wider than those for the ipsilateral eye (temporal retina) (Le Vay, Connolly, Houde & van Essen, 1985). In some portions of cortex the striped structure actually breaks *Logicon Technical Services, Inc., P.O. Box 317258, Dayton, OH 45431-7258, U.S.A. [Email [email protected]]. tArmstrong Laboratory, AL/CFHV, Wright-Patterson AFB, OH 45433-7022, U.S.A. [Email btsou(~falcon.aamrl.wpafb.af.mil].
down so that small areas of ipsilateral input are completely surrounded by large areas of contralateral input. This structure implies an asymmetry in retinal input to cortex in which nasal input dominates over temporal and, as with the human retinal cell data above, the asymmetry occurs only for areas corresponding to visual field outside of the central 40 deg. Psychophysical measurements show that these anatomical asymmetries of nasal and temporal retinal and cortical processing in the far periphery affect threshold and suprathreshold sensitivity. Far peripheral nasal retina has been found to have a higher sensitivity than temporal retina for chromatic and achromatic resolution targets, vernier acuity, and luminance and chromatic discrimination (Anderson, Mullen & Hess, 1991; Fahle & Schmid, 1988; Stabell & Stabell, 1982; Noorlander, Koenderink, den Ouden & Edens, 1983). This asymmetry may also be responsible for a breakdown in binocular processing in the far periphery. Perimetric measurements show that under optimal conditions the human achromatic visual field extends approx. 200 deg horizontally by 130 deg vertically. Of this 200 deg wide area, approx. 120 deg can be seen by both eyes at the same time. However, psychophysical measurements show that there is appreciable binocular processing only within the central 40 deg of visual field. For example, in a study of depth perception, Richards and Regan (1973) measured the extent of the stereoscopic field for a target sinusoidally modulated in
2841
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SCOTT S. GR1GSBY and BRIAN H. TSOU
disparity (see also Regan, Collewijn & Erkelens, 1986). No depth was seen at eccentricities > ~ 20 deg along the horizontal meridian. Fahle (1987) has shown a more direct correspondence between the naso-temporal asymmetry and binocular inhibition. Two distinct stimuli were presented dichoptically at corresponding points along the horizontal meridian so that the stimuli elicited rivalry. Neither stimulus dominated the inhibition in the central 40deg of visual field. However, when stimuli were presented at eccentricities > 20deg the stimulus presented to the nasal hemi-retina was seen more than twice as much as that presented to the temporal hemi-retina. Finally, binocular summation is also reduced outside of the central 40deg. Wood, Collins and Carkeet (1992) showed that binocular summation of small perimetric targets (Goldmann equivalents I, III and V) is greatly reduced in the far periphery. However, target size had an influence on the extent of summation and its rate of change with eccentricity. Binocular summation of the smallest stimuli (target I, 0.108deg) dropped fairly rapidly while that of the largest stimuli (target V, 1.724deg) stayed nearly constant. Furthermore, for the smaller targets (I and III), the amount of summation was found to be correlated with the difference between the nasal and temporal sensitivity in that larger naso-temporal differences led to smaller summation ratios. This relationship was not found for the larger target. These results imply that the amount of naso-temporal asymmetry and the extent of the binocular field may be dependent on the stimulus parameters. The purpose of the following experiment is to provide systematic measurements of monocular and binocular grating and flicker contrast sensitivity in the near and far periphery. Any effects of spatial or temporal frequency on the naso-temporal asymmetry or on binocular summation will be discussed with respect to the underlying physiology. METHODS
Photopic contrast sensitivities for sinusoidal gratings and flicker were measured as a function of horizontal eccentricity, thresholds were measured at nine eccentricities (0, _+4, _+8, + 24, _+32 deg) for both the right and left eyes and binocularly. The stimuli were generated using the VisionWorks computer graphics display system (VRG, Inc., Durham, N.H.). This system uses a PC computer and a TI 34020 graphic controller with ! 5 bits of gray-scale. The images are presented on a high resolution (1024 x 512 pixels) monitor with a 120 Hz refresh rate. The monitor was photometrically linearized and calibrated for stimulus contrast. Both the grating and flicker stimuli were generated full screen but were placed in a two-dimensional Gaussian spatial window with a = 1.5 deg. The grating stimuli were oriented vertically and were presented in a rectangular temporal envelope for 0.5 sec. The spatial fre-
quency ranged from 0.4 to 16.0 c/deg. The flicker stimuli were presented for 1.0 sec in a raised cosine temporal envelope. The flicker frequency ranged from 1.0 to 40.0 Hz. The stimuli had a mean luminance equal to that of the blank background (55 cd/m2). A screen, on which small fixation points were placed, surrounded the monitor and had the appropriate curvature to keep the observer's accommodation constant. The screen was luminance matched to the monitor, however, a small amount of chromatic mismatch was still evident. Observers used a chinrest and were instructed to fixate the appropriate point. Fixation was not monitored; however, the observers, although naive to the purpose of this experiment, were experienced at doing psychophysical experiments and at maintaining fixation for peripheral measurements. The observers had natural pupils and, for the monocular conditions, the unused eye was covered with a semi-translucent patch. Thresholds were measured using a modified Q U E S T procedure (the " Z E S T " procedure; see King-Smith, Grigsby, Vingrys, Benes & Supowit, 1994). The ZEST procedure uses a likelihood function to estimate thresholds with a yes-no staircase paradigm. Twentyfive cycles were run for each stimulus. The mean of the final probability distribution was used as an estimate of the threshold. Stimulus presentations were preceded by 0.5 sec by a warning tone. Observers were instructed to respond "yes" only to the percept of a grating (for the grating experiments) or flicker (for the flicker experiments). Repeated measures analysis of variance were done on the data. Individual contrasts were determined using t-tests. Eleven observers (10 males, 1 female; age range, 19 30yr; mean, 23.8yr) were used for the measurements. All had uncorrected Snellen acuities of 20/20 or better and normal visual fields as determined by standard Humphrey perimetery. Each observer ran a total of six 2 hr sessions (with numerous breaks) plus a I hr training session over a period of 2 weeks. Conditions were randomized between observers and days. Informed consent was obtained from all observers. RESULTS Figure 1 shows the contrast sensitivities for the grating and flicker stimuli averaged across all eleven observers. Preliminary analysis indicated no significant differences between the results for the left and right eyes or left and right fields, therefore the nasal and temporal data are an average of the two eyes. In the near periphery (4 and 8deg), binocular sensitivity is appreciably greater than nasal and temporal sensitivity--which are roughly equivalent--for both flicker and gratings. In the far periphery (24 and 32 deg), temporal retinal sensitivity for flicker has decreased slightly compared to nasal sensitivity but binocular sensitivity is still appreciably greater than either. However, temporal retinal sensitivity for gratings has dropped significantly below nasal sensitivity and binocular sensitivity is now effectively the same
C O N T R A S T SENSITIVITY IN T H E P E R I P H E R Y
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F I G U R E 1, Monocular and binocular grating and flicker contrast sensitivities in the fovea and at four peripheral eccentricities.
as nasal sensitivity alone. These findings are further analyzed below. In Fig. 2(a), the logarithm of the ratio of the nasal to temporal retinal sensitivity is plotted as a function of eccentricity and spatial frequency. The corresponding plot for flicker frequency is shown in Fig. 2(b). Pairwise comparisons were done for all of the data points. Significant differences (P ~< 0.05) between nasal and
temporal sensitivities are shown as solid circles. Open circles indicate no statistically significant difference at the 0.05 level. Table 1 shows the A N O V A results comparing nasal and temporal retinal sensitivity for (a) gratings and (b) flicker. N o significant differences were found between nasal and temporal sensitivity at 4 deg for gratings or flicker ( P / > 0.2660). A significant difference (P = 0.0408)
2844
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CONTRAST SENSITIVITY IN THE PERIPHERY
2845
TABLE 1. Analysis of variance results for nasal vs temporal sensitivity for gratings and flicker Eccentricity
Nasal vs temporal sensitivity
Mean A*
Interaction w/frequency
(a) Gratings
4deg 8 deg 24deg 32 deg
F(I, F(I, F(I, F(I,
10)= 1.39 10) = 5.07 10) = 64.78 10) = 37.39
P P P P
=0.2660 = 0.0408 = 0.0001 = 0.0001
0.037 0.041 0.344 0.449
F(7, 70) = 0.16 F(6, 60) = 0.92 F(4, 40) = 9.64 F(3, 30) = 26.22
P P P P
=0.9914 = 0.4858 = 0.0001 = 0.0001
F(I, F(I, F(1, F(1,
10) = 0.07 10)= 1.96 10) = 36.57 10) = 28.23
P P P P
= 0.7995 =0.1921 = 0.0001 = 0.0003
0.005 0.023 0.120 0.185
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P P P P
= 0.7468 =0.1504 = 0.5600 = 0.2352
(b) Flicker
4 deg 8deg 24 deg 32 deg
70) = 0.61 70) = 1.60 70) = 0.84 70) = 1.36
*Mean A is the difference in log units between nasal and temporal retinal sensitivity.
was found at 8 deg for gratings but this difference was very small (mean difference across frequencies = 0.041 log units). No significant difference was found between nasal and temporal sensitivity at 8 deg for flicker (P =0.1921). At 24 and 32deg, nasal sensitivity was found to be significantly greater than temporal sensitivity for both gratings and flicker (P ~< 0.0003). Table 1 also shows that this sensitivity difference in the far periphery has an interaction with spatial frequency (P ~< 0.0001) in that the naso-temporal difference increased with increasing spatial frequency. There was no significant differential effect of flicker frequency (P ~> 0.2352). Figure 3(a,b) shows the binocular summation ratios (binocular/nasal sensitivity) as a function of eccentricity and frequency for gratings and flicker, respectively. Table 2 shows the A N O V A results for the binocular summation comparisons (binocular vs nasal sensitivity) for (a) gratings and (b) flicker in the near and far periphery. Significant binocular summation (P ~ 0.0001) was found in the near periphery (4 and 8 deg) for both grating and flicker stimuli. There was no significant interaction with frequency for grating stimuli (P ~> 0.2164) but the flicker stimuli did show an interaction (P = 0.0032) at 4 deg eccentricity. The interaction is due to a slightly reduced amount of summation at the highest flicker frequencies (24 and 40 Hz) and does not appear to be a major effect. For gratings in the far periphery, a significant (P = 0.0263) but reduced amount of summation was found at 24 deg eccentricity but no significant summation was found at 32 deg (P = 0.2355). Significant levels (P ~< 0.0036) of summation were found at both 24 and 32 deg for flicker. There was no effect of spatial or flicker frequency on binocular summation in the far periphery (P >/0.2722). The relationship between the extent of the n a s o temporal asymmetry and the amount of binocular summation can be seen in Fig. 4. Regression lines have been fit through the data for gratings and flicker (R 2 = 0.507, s l o p e = - - 0 . 4 1 9 for gratings and R 2 = 0 . 6 7 4 , slope = - 0 . 7 9 2 for flicker). The plot shows that for both flicker and gratings the amount of summation decreases as the naso-temporal sensitivity differences increases and the amount of summation is effectively zero when the
sensitivity difference is > ~ 2 : 1 . However, the relationship is fairly irregular and there is a large range of summation ratios even when nasal and temporal retinal sensitivities are similar. DISCUSSION The results are consistent with previous studies in showing a large asymmetry between nasal and temporal retinal sensitivity beyond 20 deg eccentricity. However, the asymmetry seems to be larger for gratings than flicker and shows an effect of spatial but not flicker frequency. There are at least three possible causes for the spatial frequency dependent difference of nasal and temporal retinal sensitivity in the far periphery: (1) the difference in photoreceptor cell density (Curcio et al., 1990), (2) the difference in ganglion cell density (Curcio & Allen, 1990), or (3) the difference in ganglion cell receptive field size (Spillmann et al., 1987) between the two hemi-retinae. Anderson et al. (1991) have shown that the limit of spatial resolution in the periphery is most likely due to ganglion cell density and not receptor density or optical factors. The Nyquist frequency limit of the ganglion cell mosaic as a function of eccentricity is qua.litatively similar to the drop in resolution. Also, when ganglion cell spatial acuity is compared with the Nyquist limits for individual ganglion cells as a function of eccentricity, spatial acuity exceeds the cell Nyquist limit at eccentricities beyond 15 deg. This, Anderson et al. suggest, means that the limit to resolution in the periphery is due to the sampling density of the ganglion cells and not the individual cell receptive field size. Therefore, the asymmetry they find in spatial resolution between the temporal and nasal hemi-retinae is simply a reflection of the asymmetry between the ganglion cell densities. The above findings suggest that it is the ganglion cell density and not ganglion cell receptive field size or photoreceptor density that is the predominant factor in limiting spatial resolution in the far periphery. This can be used to account for the asymmetry in the nasal and temporal retinal contrast sensitivity measurements found here. Virsu and R o v a m o (1979) have shown that the shape of the contrast sensitivity curve is related to the
2846
SCOTT S. G R I G S B Y and B R I A N H. TSOU
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CONTRAST
2847
SENSITIVITY IN THE PERIPHERY
T A B L E 2. A n a l y s i s of v a r i a n c e results for b i n o c u l a r vs nasal sensitivity for gratings a n d flicker Eccentricity
Binocular summation
M e a n A*
I n t e r a c t i o n w/frequency
(a) Gratings 4 8 24 32
deg deg deg deg
F(1, F(1, F(I, F(1,
10) 10) 10) 10)
= = = =
77.61 234.90 6.78 1.59
P P P P
= = = =
0.0001 0.0001 0.0263 0.2355
0.209 0.177 0.083 0.045
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1.41 0.80 0.32 0.48
P P P P
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0.2164 0.5740 0.8973 0.7484
F(I, F(I, F(1, F(1,
10) 10) 10) 10)
= = = =
130.71 109.59 54.81 14.23
P P P P
= = = =
0.0001 0.0001 0.0001 0.0036
0.245 0.212 0.157 0.091
F(7, F(7, F(7, F(7,
70) 70) 70) 70)
= = = =
3.44 2.12 1.28 0.98
P P P P
= = = =
0.0032 0.0522 0.2722 0.4499
(b) Flicker 4 8 24 32
deg deg deg deg
* M e a n A is the difference in log units between b i n o c u l a r and nasal retinal sensitivity.
far temporal hemi-retina as compared to the nasal hemi-retina due to the reduced ganglion cell density. Differences in ganglion cell density should not affect the shape of the flicker sensitivity curve in that density alone would not be expected to affect the temporal processing characteristics of the individual ganglion cells. However, different amounts of pooling of ganglion cell signals could lead to differences in maximal sensitivity (unless the signals are somehow renormalized), i.e. less pooling would mean a lower signal/noise ratio and therefore an overall frequency-nonspecific decrease in sensitivity such as that found here. The summation data are also consistent with other studies in finding reduced binocular processing in the far periphery. Figure 5 shows that the average amount of binocular summation across all spatial frequencies drops off rapidly in the periphery and is near zero by 24 deg eccentricity. Average flicker summation shows a less rapid drop off but it too is significantly reduced by 32 deg eccentricity. As shown in Fig. 4, this loss of binocular summation in the far periphery is correlated
ganglion cell receptive field spacing; increased receptive field spacing leads to a decreased maximal sensitivity, a lower peak frequency and a lower high-frequency cutoff. These are the same effects found in the grating sensitivity plots of Fig. 1 for 24 and 32 deg eccentricity; contrast sensitivity for the temporal hemi-retina shows a reduction in the maximal sensitivity, the peak frequency, and the cut-off frequency as compared to the nasal hemi-retina. This implies that the shape of the contrast sensitivity curves are a reflection of the underlying ganglion cell density, and it is this difference in the shape of the contrast sensitivity curves which leads to the spatial frequency dependency of the nasa-temporal asymmetry. Ganglion cell density may also explain the frequency independence of the nasa-temporal asymmetry for flicker. Temporal retinal sensitivity is reduced compared to nasal sensitivity for all flicker frequencies by approximately the same amount. This can be seen in the flicker results of Fig. 1 for 24 and 32 deg eccentricity. This could simply be attributed to a reduced signal strength for the 0.4
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Log(Nasal/Temporal) F I G U R E 4. Scatter p l o t s h o w i n g the r e l a t i o n s h i p between the a m o u n t o f b i n o c u l a r s u m m a t i o n a n d the a m o u n t o f n a s a - t e m p o r a l a s y m m e t r y . R e g r e s s i o n lines are s h o w n i n d i v i d u a l l y for the g r a t i n g a n d flicker d a t a (R 2 = 0.507, slope = - 0 . 4 1 9 for g r a t i n g s a n d R 2 = 0.674, slope = - 0 . 7 9 2 for flicker).
2848
SCOTT S. GRIGSBY and BRIAN H. TSOU
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with the extent of the naso-temporal sensitivity asymmetry for both flicker and gratings. While a correlation does not imply a cause-and-effect relationship, the results suggest that binocular processing drops off because nasal sensitivity starts to dominate over temporal sensitivity and, therefore, the signals are no longer useful for binocular processing. Another possible physiological correlate for the lack of binocular processing especially for spatial stimuli may be found in the topographic organization of the parvocellular layers of the lateral geniculate nucleus (LGN). Connolly and van Essen (1984), using data of their own and that of Malpeli and Baker (1975), constructed two-dimensional topographic maps of the separate layers of the LGN of macaque monkey. The two magnocellular layers (LGN layers 1 and 2) as well as parvocellular layers 3 and 6 have visual field representations extending out to ~80 deg eccentricity and beyond. However, the field representations for parvocellular layers 4 and 5 do not extend much beyond 20 deg eccentricity. Because both the extent of the binocular field-of-view; as evidenced by the summation, stereo and rivalry data, and the extent of the topographic boundaries of layers 4 and 5 correspond only to the central 40 deg of visual field, the hypothesis can be made that parvocellular layers 4 and 5 have a large role in relaying binocular information to cortex. REFERENCES Anderson, S. J., Mullen, K. T. & Hess, R. F. (1991). Human peripheral spatial resolution for achromatic and chromatic stimuli: Limits imposed by optical and retinal factors. Journal of Physiology, 442, 47~64. Connolly, M. & van Essen, D. (1984). The representation of the visual field in parvicellular and magnocellular layers of the lateral geniculate nucleus in the Macaque monkey. Journal of Comparative Neurology, 226, 544-564. Curcio, C. A. & Allen, K. A. (1990). Topography of ganglion cells in the human retina. Journal o[" Comparative Neurology, 300, 5-25.
Curcio, C. A., SIoan, K. R., Kalina, R. E. & Hendrickson, A. E. (1990). Human photoreceptor topography. Journal of Comparative Neurology, 292, 497 523. FaMe, M. (1987). Naso-temporal asymmetry of binocular inhibition. Investigative Ophthalmology & Visual Science, 28, 1016-1017. Fahle, M. & Schmid, M. (1988). Naso-temporal asymmetry of visual perception and of the visual cortex. Vision Research, 28, 293 300. King-Smith, P. E., Grigsby, S. S., Vingrys, A. J., Benes, S. C. & Supowit, A. (1994). Efficient and unbiased modifications of the QUEST threshold method: Theory, simulations, experimental evaluation and practical implementation. Vision Research, 34, 885 912. LeVay, S., Connolly, M., Houde, J. & van Essen, D. C. (1985). The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey. Journal of Neuroscience, 5, 486-50 I. Malpeli, J. G. & Baker, F. H. (1975). The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta. Journal of Comparative Neurology, 161, 569 594. Noorlander, C., Koenderink, J. J., den Ouden, R. J. & Edens, B. W. (1983). Sensitivity to spatiochromatic colour contrast in the peripheral visual field. Vision Research, 23, 1 11. Regan, D., Collewijn, H. & Erkelens, C. (1986). Necessary conditions for motion in depth perception. Investigative Ophthalmology and Visual Science, 27, 584-597. Richards, W. & Regan, D. (1973). A stereo field map with implications for disparity processing. Investigative Ophthalmology, 12, 904 909. Spillmann, L., Ransom-Hogg, A. & Oehler, R. (1987). A comparison of receptive and perceptive fields in man and monkey. Human Neurobiology, 6, 51 62. Stabell, U. & Stabell, B. (1982). Color vision in the peripheral retina under photopic conditions. Vision Research, 22, 839 844. Virsu, V. & Rovamo, J. (1979). Visual resolution, contrast sensitivity, and the cortical magnification factor. Experimental Brain Research, 3Z 475 494. Wood, J. M., Collins, M. J. & Carkeet, A. 0992). Regional variations in binocular summation across the visual field. Ophthalmic and Physiological Optics, 12, 46 51.
Acknowledgements
This work was supported by AF workunit 71841158 of Armstrong Laboratory (Wright-Patterson Air Force Base, Ohio). The authors would like to thank Beth Rogers-Adams and Chuck Goodyear of Logicon Technical Services, Inc (Dayton, Ohio) for their assistance on this study.