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Spatial resolution across the macaque retina
$3.00 + 0.00 0042-6989/90 Copyright 0 1990 Pergamon Press plc
1990 Vision Rex. Vol. 30. No. 7, pp. 985-991, Printed in Great Britain. All rights reserved
SPATIAL
RESOLUTION
ACROSS THE MACAQUE
RETINA
WILLIAM H. MERIGA~ and LAURENCE M. KATZ* Department of Ophthalmology
and Center for Visual Science, University of Rochester Medical Center, Rochester, NY 14642, U.S.A.
(Receioed 10 October 1989, in revisedform 11 December 1989) Abstract-Grating acuity was measured as a function of eccentricity from the fovea in two macaques. A vertical-horizontal o~~tation di~mination was used to determine acuity, and the retinal locus of the test grating was controlled by training them to fixate a spot placed at various distances from the stimulus. Their head was fixed in place and fixation was monitored with a scleral search coil. The acuity of monkeys across the retina was similar to that previously measured in human subjects, reaching a peak of about 38 c/deg at the fovea, and decreasing about IO-fold by 30 deg eccentricity. Acuity was slightly higher in the temporal than in the nasal visual field. The shape of the acuity-eccentricity function suggested a dependence on cone density near the fovea, and on the density of P ganglion cells at eccentricities beyond 10 deg. Existing physiological data suggest the possibility that macaque acuity may also be limited in part by spatial averaging across the receptive field of retinal ganglion cells. Acuity
Sampling density
Cones
Ganglion cells
INTRODUCIION
Visual acuity falls off steeply with distance from the fovea to the periphery of the visual field (Wertheim, 1894), and numerous studies have attempted to relate this decline to optical or anatomical features of the eye. Optical limitations are important primarily in central vision, as indicated by the close correspondence between central visual acuity and the 55 to 6Ocjdeg limit imposed by the optics of the eye ~Camp~ll & Green, 1965; Campbell & Gubisch, 1966). Peripheral visual acuity, on the other hand, reaches much lower spatial frequencies than are passed by the eye’s optics (Millodot, Johnson, Lamont & Leibowitz, 1975). Cone photoreceptor sampling also appears to be an important determinant of central acuity (Williams & Coletta, 1987), but cone density seems much too high to limit peripheral acuity (Thibos, Walsh & Cheney, 1987a). Ganglion cell density (Thibos, Cheney & Walsh, 1987b) or spatial averaging by visual neurons (related to dendritic morphology or receptive field dimensions) might limit peripheral visual acuity, but, at present, there are not sufficient data for human eyes to make this dete~ination. *Present address: Department of Ophthalmology, Ford Hospital, Detroit, MI 48202, U.S.A.
Henry
Macaque monkey
Physiological and anatomical data are available for macaque ganglion cells, and therefore, the present study examined visual acuity as a function of eccentricity in the macaque monkey. Macaques show striking parallels to humans in many aspects of visual anatomy and function (Shapley & Perry, 1986; Merigan, 1989), and this is especially true for retinal structure (Perry, Oehler & Cowey, 1984; Rodieck, 1988). While it is more difficult to obtain threshold measures in macaques than in humans, they have certain advantages over humans for relating resolution limits to visual system characteristics. One advantage is that macaques have a more pronounced naso-temporal asymmetry in cone density than humans (Curcio, Sloan, Packer, Hendrickson & Kalina, 1987). This asymmetry is very useful for correlating acuity with morphological properties that could limit it. A second advantage isthat physiolo~~l measures relevant to visual acuity, such as receptive field center size, have been reported for the macaque retina, geniculate and visual cortex (e.g. Crook, Lange-Malecki, Lee BEValberg, 1988), but not for humans. Furthermore, some anatomical measures, such as ganglion cell density, are more precisely known for the macaque than the human retina. Other properties of the eye, such as cone photoreceptor density and ganglion cell dendritic morphology, are known for both the human and macaque. 985
WILLIAM H. MERIGAN and LAURENCEM. KATZ
986
Peripheral visual acuity has not previously been measured in macaques. and the present results indicate that it is quite similar to that of humans. furthermore, the density of one class of retinal ganglion cells appears to match (and to this extent may iimit) peripheral acuity. Existing physiological data. while limited, suggest that averaging within receptive fields may also play some role in limiting macaque acuity.
‘2’ I
METHODS
I
Subjects
The subjects were two adult, female macaque monkeys (Macaca nemestrina). They had free access to Purina monkey chow, supplemented regularly with fresh fruit, and they were water deprived 5 days each week for approximately 20 hr before threshold testing. All thresholds were measured monocularly for the right eye of each subject during controlled fixation. Neither monkey was more than 0.5D myopic in its right eye. After initial training on the procedure described below, each monkey was anesthetized with isoflurane and a scleral search coil implanted in the right eye (so that eye position could be monitored) and a stainless steel sleeve attached to the skull (so that the head could be immobilize) (Judge et al., 1980). The fixation target, a red spot from a HeNe laser, was initially placed on the test grating and then gradually moved away over several sessions. Apparatus and procedure
The monkeys were seated in an acrylic chair facing a high resolution display oscilloscope (Tektronix 606 with P-31 phosphor). The mean luminance of the display was maintained at 16 cd/m* and it was viewed through a circular aperture (dimensions below) in an unilluminated white surround. A dim red fixation spot was presented on the surround to control the location of fixation relative to the test grating (Fig. 1). Acuity was tested with an orientation discrimination rather than a detection paradigm to minimize the use of cues to grating presence produced by stimuli beyond the resolution limit. Test stimuli were vertical or horizontal sinusoidal gratings of 0.55 Michelson contrast (L,, - ~~i”f~~~~+ Lma), presented with a smoothed onset (l/2 cycle of a raised cosine of 0.5 Hz). Each trial began, after a four second intertrial interval, with presentation of the dim
/
iI73 “II
i
Fig. 1. Schematic of the test procedure. The seated monkey monocularly viewed a red fixation spot (F), located at the testing eccentricity (0) from the nearest edge of the grating stimulus (S). The monkey’s head was fixed in place (H) and fixation was monitored with a scleral search coil.
red fixation spot. When the monkey fixated within an electronic window extending approx. f0.33 deg from the fixation spot, a 4500 Hz tone was presented and stimulus onset was initiated, The tone remained on for 1.8 see, and then went off, signalling the o~rtunjty to respond. The stimulus was present until either a response was made or the monkey’s fixation moved outside of the electronic window. Responses to the left button on the response panel were correct when the stimulus was a vertical grating, and to the right pushbutton when a horizontal grating was present. Correct choices were rewarded with fruit juice, while errors-were followed by presentation of a 6 set buzzing tone. If the monkey moved its fixation locus outside the window before responding, or responded on a pushbutton during the tone, the stimulus was removed and the tone extinguished, and after a 3 set beeping tone the intertrial interval was restarted. The spatial frequency of the test grating was varied according to a staircase, decreasing by one step (0.3 octave) after each error, and increasing, with probability 0.33, after each correct choice. Daily sessions consisted of 200 trials, and acuity thresholds were taken at 75% correct responding either by linear interpolation, or from probit fits to the daily psychometric functions (Finney, 1971). Acuity was tested monocularly along the horizontal meridian of the right eye in monkey 676, and along the superior and temporal meridia in monkey 675. Measurements were
Spatial resolution across macaque retina
made at eccentricities of 0, 3, 6, 12, 20, and in some cases 25 or 30deg (visual subtense of the fixation spot from the nearest edge of the stimulus). The test target was 185 cm from the observer for eccentricities of 0,3, and 6 deg and 93 cm for eccentricities beyond 6 deg. Diameter of the stimulus was 0.5 deg for 0 deg eccentricity, 1 deg for 3 and 6 deg eccentricity, 1.5 deg for 12 deg, and 3 deg for 20, 25 and 30 deg eccentricity. Thus, the stimulus was always approximately 20 cycles of a just resolvable grating. RESULTS
Figure 2 illustrates representative psychometric functions for monkey 676 for acuity measures along the horizontal nasal field meridian. The data points of each psychometric function are fitted by probit curves (Finney, 1971). It can be seen that threshold spatial frequency (taken as the intersection of the probit function with 75% correct identification) decreased in an orderly fashion with eccentricity from the fovea, but that the form of the psychometric function did not change with eccentricity. Mean acuity thresholds ( f SE) for monkey 676 along the horizontal meridian of the right eye are shown in Fig. 3, and for monkey 675 along the temporal and superior meridia of the right eye in Fig. 4. The dotted curve in each figure represents the Nyquist frequency calculated for cone density in the rhesus monkey retina (Perry & Cowey, 1985). Dashed lines indicate Nyquist frequencies calculated for On or Off P type ganglion cell density in the rhesus monkey retina (Perry & Cowey, 1985). Calcu1
9x7
30
30
0
E~ntfici~
(degf
Fig. 3. Mean acuity thresholds ( f SE) for monkey 676 along the horizontal meridian of the right eye. The dotted curve represents the average Nyquist frequency for cone density along the horizontal meridian of the rhesus monkey retina (Perry & Cowey, 1985). Dashed lines indicate average Nyquist frequencies calculated for the density of On or Off P ganglion cells along the horizontal meridian of the rhesus monkey retina (Perry et al., 1984).
lation of the Nyquist frequency is described in the Discussion. Measured acuities are in close agreement with Nyquist frequencies calculated for cone density out to eccentricities of about 10 deg, and with the Nyquist frequency calculated for ganglion cell density beyond 10 deg. DISCUSSION
This study demonstrates that macaque acuity, like that of humans, decreases very sharply with distance from the fovea, and that it is both quantitatively and qualitatively similar to that of humans. The decline in macaque acuity with distance from the fovea is steeper along nasal and superior visual field meridia than along the temporal visual field. Measured acuities closely matched cone Nyquist frequencies out to an eccentricity of approximately 10 deg, but matched the Nyquist frequency for On or Off P
4oc. 5 SpEdOFmque”cy
(c/&ig;o
Fig. 2. Representative psychometric functions for the spatial resolution of monkey 676 along the temporal visual field meridian. Squares (0 deg ~nt~~ty), circles (3 deg eccentricity), triangles (12 deg eccentricity), diamonds (20 deg eccentricity). Probit functions were fit to the data for each eccentricity. Thresholds were taken as the value corresponding to 75% correct. indicated by the dashed line.
0
30
0
30
Eccentricity (deg) Fig. 4. Mean acuity (&SE) for monkey 675 along the superior and temporal field meridia of the right eye. Theoretical curves are as in Fig. 3.
YXP
WILLIAM i-1. MEKIGANand LAURENCEM. KATZ
ganglion cells at greater eccentricities. These results imply that the major limitations on primate spatial vision may already be present in the retina, in the form of limitations on spatial
sampling of the visual image. In the central retina this limit is related to cone sampling density. and in peripheral retina to ganglion cell sampling density. The match between Nyquist frequency and resolution thresholds indicates that no further loss in resolution takes place beyond the retina, as might be expected if convergence or spatial averaging of neuronal signals in central visual pathways further limited acuity. Relation of macaque to human visual acuity The anatomy of the eye and retina are very similar in human and macque. The human eye is slightly larger, approximately 24 mm in length compared to about 20mm for the macaque (Rolls & Cowey, 1970). The larger eye results in a slightly greater retinal magnification factor (relation of mm of retinal extent to degrees of visual angle) in the human [0.291 mm/deg, Perry et al. (1984)] compared to the rhesus macaque [0.223 mm/deg, Perry et al. (1985)]. Cone density as a function of eccentricity is very similar in the rhesus monkey (Perry & Cowey, 1985), pigtailed monkey (Packer, Hendrickson & Curcio, 1989b), and in humans (Curcio et al., 1987) for eccentricities outside the fovea. However, cone density measurements for the fovea are quite variable from study to study. For example, Perry and Cowey (I 985) reported average fovea1 cone densities for the rhesus monkey of 140,500, while Packer et al. (1989b) found a mean of 210,O~ cones/mm2 in the pigtailed macaque. Much of the difference between these results appears to be due to the larger averaging area (90 x 90 u) used by Perry and Cowey than that used by Packer et al. (37 x 54 u). On the other hand, there do appear to be substantial differences in foveal cone density even between individuals from the same study. Curcio et al. (1987) found a 2.9-fold range around a mean fovea1 density of 161,900 cones/mm2 in a sample of four human retinas. Packer, Williams, Sekiguchi, Coletta and Galvin (1989a) reported a 1.4-fold range around a mean fovea1 cone density of 2 10,000 cones/mm’ in a sample of three pigtailed macaque retinas. It should be noted that because of the greater retinal magnification factor in humans, the mean cone density per degree of visual angle in the above studies was slightly higher in humans
than macaques. Thus, the human and macaque retinas are very similar, although the human retina has a slightly higher angular density of fovea1 cones. Human and macaque acuity were comparable in the present study, a result that confirms numerous studies of spatial vision in primates. Perhaps the most detailed cross-species comparison of acuity was that of Cavonius and Robbins (1973) who measured the acuity of macaques and humans over an 8 log unit range of luminances, using Landolt rings as test targets. They found that human and macaque acuity were very similar over a 4 log unit range of luminances, but that humans reached slightly higher acuity at the highest luminances, while macaques had superior acuity at the lowest tested luminances. The reported differences at high luminances were small (about 36%) and appear to be within the range of inter-individual differences found for central cone density. The spatial contrast sensitivity of adult macaques is also virtually identical to that of humans tested under the same conditions (DeValois, Morgan & Snodderly, 1974; Merigan, 1989). Thus, the anatomy and spatial resolution of the macaque eye are sufficiently like that of humans that an analysis, in macaques, of what limits acuity is likely to be directly applicable to human vision. Optical and luminance limits on visual acuity Central visual acuity in humans is limited to about 60 c/deg by optical degradation (Campbell & Green, 1965; Cambell & Gubisch, 1966), approximately the same limit imposed by the sampling density of photoreceptors (Williams, 1985). With eccentricity from the fovea, optical degradation of the visual image has been reported to decline more slowly than visual resolution (Jennings & Charman, 1981). Thus, optical quality appears not to limit the peripheral spatial resolution of humans, and the same is likely to be true for macaques. Spatial resolution is also limited by quanta1 fluctuations in the stimulus (Banks, Geisler & Bennett, 1987). Contrast thresholds decrease in proportion to the square root of luminance (Rose, 1942), resulting in a marked drop in spatial resolution. Because of this relationship, stimulus luminance and contrast must be reasonably high if acuity is to be limited primarily by retinal sampling density. In the present study, the stimulus luminance (16 cd/m’) was sufficiently high that macaque acuity is
Spatial resolution across macaque retina
nearly asymptotic at this luminance (Cavonius & Robbins, 1975). Sampling density limits on visual acuity
According to the sampling theorem, spatial resolution in one dimension is limited by sampling density such that the highest frequency that can be unambiguously imaged (the Nyquist frequency) is half the frequency of the array of detectors (Bracewell, 1975). For twodimensional arrays with hexagonal packing of receptors, the Nyquist frequency is F nyq = (0.5)(0.223)(1.15470)1/2
where D is receptor density per square mm, 0.223 is the conversion from mm of macaque retina to degrees of visual angle, and 1.1547 is the correction for hexagonal packing (Snyder & Miller, 1977). Because the Nyquist frequency represents a theoretical boundary for the veridical representation of an image, it is probably an important limit for such visual functions as recognizing objects or reading text, where ambiguity about stimulus interpretation would seriously degrade visual performance. On the other hand, it is clear that under some circumstances vertical-horizontal discrimination of grating orientation can be done at spatial frequencies beyond the Nyquist limit. For example, it was demonstrated by Williams and Coletta (1987) that human observers could discriminate the orientation of gratings up to spatial frequencies approximately 1.5 times the nominal Nyquist frequencies. More recently, Packer et al. (1989b) showed that separate stimulation of long or middle wavelength cones, which greatly reduces the average Nyquist frequency, did not decrease visual acuity. However, resolution beyond the Nyquist frequency was not apparent in the present study, in which Nyquist frequency was calculated from published counts of ganglion cells density (Perry et al., 1984) in which the extrafoveal displacement of ganglion cells was not taken into account. Ganglion cell density may be adjusted in later studies (e.g. Wassle, Grunert, Rohrenbeck & Boycott, 1989) by using the length of fibers of Henle (Schein, 1988; Perry & Cowey, 1988) to estimate ganglion cell displacement, but such an adjustment will have little effect on the calculation of Nyquist limits for ganglion cells. At eccentricities beyond 10 deg, measured visual acuity in this and previous studies (e.g. Wertheim, 1894) falls well below the Nyquist frequency calculated for cone photoreceptors.
989
Since ganglion cells are less numerous than cones beyond 10 deg eccentricity, we compared acuities beyond 10 deg to the Nyquist calculated for P type retinal ganglion cells (which make up about 80% of ganglion cells (Perry et al., 1984). We considered On and Off ganglion cell matrices independent, on the basis of the calculation (Schein & DeMonasterio, 1987; Wassle, 1989) that there are somewhat over two ganglion cells for each central cone in the primate, and, thus, that On and Off ganglion cells may receive independent input from each cone. It can be seen in Figs 3 and 4 that acuity beyond 10 degrees agrees well with predictions from the Nyquist frequency for On or Off P ganglion cells [also see Thibos et al. (1987b)], and that meridional differences in ganglion cell density are reflected in different acuities. Since M ganglion cells make up only about 10% of retinal ganglion cells (Perry et al., 1984) the Nyquist frequency for the matrix of On or Off M cells would be lower by approximately 3 fold than that calculated here for P cells. While such a matrix could subserve many visual capacities, it is unlikely that it could mediate tasks requiring the visibility of high spatial frequencies, such as reading small text at a distance. Spatial averaging and the resolution limit
Spatial resolution can also be limited by spatial averaging across the aperture of neural elements (Snyder & Miller, 1977; Barlow, 1981). It is already clear from the data of Figs 3 and 4 that spatial averaging could not uniquely limit primate visual resolution, since there appear to be no further constraints on acuity beyond those due to retinal sampling density. However, it is possible that acuity might be jointly limited by sampling density and spatial averaging. Averaging cannot limit resolution when the summation aperture is small relative to the spacing of neural detectors. This is the case for photoreceptors in the monkey retina, whose aperture is shown by the data of Thibos et al. (1987a) to limit detection to about 130 c/deg in the fovea, and about 45 c/deg at 20 deg eccentricity. This is probably also true for P ganglion cells in the central retina, since their receptive field centers appear to be driven by single cones (Shapley & Perry, 1987). However, larger summation areas resulting from convergence can limit spatial resolution because of either the reduced sampling density of the matrix of second level neurons, or their greater receptive
990
WILLIAM H. MERIGAN
field areas (which produces lower resolution in those cells with linear spatial summation). Receptive field size in the cat retina has been shown to be well predicted by the dendritic field size of retinal ganglion cells (Peichl & Wassle, 1983). It would be most useful if such a relationship were also known for the primate retina, because excellent data are available for retinal ganglion cell dendritic fields in both macaque (Perry et al., 1984), and human (Rodieck et al., 1985). These data indicate, among other things, that the dendritic fields of M ganglion cells (which project to magnocellular layers of the lateral geniculate) are about 3 times greater in diameter than those of P ganglion cells (which project to parvocellular layers of the geniculate). Unfortunately, the relation of dendritic to receptive field size is not known for the primate, and, thus, this anatomical data cannot be used to calculate limits on acuity. The most direct way to determine the effects of spatial averaging in the primate visual pathway is to measure the spatial resolution of single cells, or, in the case of linearly summating cells, the size of the receptive field center. One should bear in mind that since such measures do not reflect sampling density, they cannot be used to infer the resolution of visual pathways. Crook et al. (1988) report such data for retinal ganglion cells of the macaque. They found that the aperture limitation on resolution in P cells was only slightly below the psychophysical resolution measured in the present study. A similar result has been found in the macaque lateral geniculate nucleus by Kaplan and Shapley (1982), Hicks et al. (1983), Derrington and Lennie (1984) Blakemore and VitalDurand (1986), and in macaque striate cortex by Hawken and Parker (1986) and Blakemore and Vital-Durand (1983). Unfortunately, the basis of the spatial averaging implied by the size of receptive field centers or the resolution of single neurons remains unclear. If central macaque P cells actually receive input to their receptive field centers from single cones (Shapley & Perry, 1986), receptive field centers should be much smaller than reported in the above studies, and resolution much higher. The apparently large receptive field centers for central P cells reported in these studies probably reflect a joint effect of optical degradation and eye movements. On the other hand, the reported center size for M cells and more peripheral P cells may be correct since they likely receive input from multiple cones, and
and
LAURENCE M. KATZ
optical and eye movement artifacts are less likely to have affected these measurements. The agreement between measured or calculated resolution for such cells is reasonably close to the psychophysical acuity measured in this study. This agreement suggests that spatial resolution in the macaque may be partially limited by spatial averaging over the receptive field, in addition to the previously described sampling density limitations. Ackno~vledgemenu-We
thank Cheryl Ruff-Neri for assistance in testing monkeys and Beverley Katz for serving as an observer in this experiment. Drs William Newsome and Robert Wurtz provided instruction on the technique of eye coil placement, and Drs Tatiana Pasternak and David R. Williams commented on the manuscript. This research was supported by grants NSF 8518858, ES01247, EY01319 and AFOSR 89-004 I
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1990 Vision Rex. Vol. 30. No. 7, pp. 985-991, Printed in Great Britain. All rights reserved
SPATIAL
RESOLUTION
ACROSS THE MACAQUE
RETINA
WILLIAM H. MERIGA~ and LAURENCE M. KATZ* Department of Ophthalmology
and Center for Visual Science, University of Rochester Medical Center, Rochester, NY 14642, U.S.A.
(Receioed 10 October 1989, in revisedform 11 December 1989) Abstract-Grating acuity was measured as a function of eccentricity from the fovea in two macaques. A vertical-horizontal o~~tation di~mination was used to determine acuity, and the retinal locus of the test grating was controlled by training them to fixate a spot placed at various distances from the stimulus. Their head was fixed in place and fixation was monitored with a scleral search coil. The acuity of monkeys across the retina was similar to that previously measured in human subjects, reaching a peak of about 38 c/deg at the fovea, and decreasing about IO-fold by 30 deg eccentricity. Acuity was slightly higher in the temporal than in the nasal visual field. The shape of the acuity-eccentricity function suggested a dependence on cone density near the fovea, and on the density of P ganglion cells at eccentricities beyond 10 deg. Existing physiological data suggest the possibility that macaque acuity may also be limited in part by spatial averaging across the receptive field of retinal ganglion cells. Acuity
Sampling density
Cones
Ganglion cells
INTRODUCIION
Visual acuity falls off steeply with distance from the fovea to the periphery of the visual field (Wertheim, 1894), and numerous studies have attempted to relate this decline to optical or anatomical features of the eye. Optical limitations are important primarily in central vision, as indicated by the close correspondence between central visual acuity and the 55 to 6Ocjdeg limit imposed by the optics of the eye ~Camp~ll & Green, 1965; Campbell & Gubisch, 1966). Peripheral visual acuity, on the other hand, reaches much lower spatial frequencies than are passed by the eye’s optics (Millodot, Johnson, Lamont & Leibowitz, 1975). Cone photoreceptor sampling also appears to be an important determinant of central acuity (Williams & Coletta, 1987), but cone density seems much too high to limit peripheral acuity (Thibos, Walsh & Cheney, 1987a). Ganglion cell density (Thibos, Cheney & Walsh, 1987b) or spatial averaging by visual neurons (related to dendritic morphology or receptive field dimensions) might limit peripheral visual acuity, but, at present, there are not sufficient data for human eyes to make this dete~ination. *Present address: Department of Ophthalmology, Ford Hospital, Detroit, MI 48202, U.S.A.
Henry
Macaque monkey
Physiological and anatomical data are available for macaque ganglion cells, and therefore, the present study examined visual acuity as a function of eccentricity in the macaque monkey. Macaques show striking parallels to humans in many aspects of visual anatomy and function (Shapley & Perry, 1986; Merigan, 1989), and this is especially true for retinal structure (Perry, Oehler & Cowey, 1984; Rodieck, 1988). While it is more difficult to obtain threshold measures in macaques than in humans, they have certain advantages over humans for relating resolution limits to visual system characteristics. One advantage is that macaques have a more pronounced naso-temporal asymmetry in cone density than humans (Curcio, Sloan, Packer, Hendrickson & Kalina, 1987). This asymmetry is very useful for correlating acuity with morphological properties that could limit it. A second advantage isthat physiolo~~l measures relevant to visual acuity, such as receptive field center size, have been reported for the macaque retina, geniculate and visual cortex (e.g. Crook, Lange-Malecki, Lee BEValberg, 1988), but not for humans. Furthermore, some anatomical measures, such as ganglion cell density, are more precisely known for the macaque than the human retina. Other properties of the eye, such as cone photoreceptor density and ganglion cell dendritic morphology, are known for both the human and macaque. 985
WILLIAM H. MERIGAN and LAURENCEM. KATZ
986
Peripheral visual acuity has not previously been measured in macaques. and the present results indicate that it is quite similar to that of humans. furthermore, the density of one class of retinal ganglion cells appears to match (and to this extent may iimit) peripheral acuity. Existing physiological data. while limited, suggest that averaging within receptive fields may also play some role in limiting macaque acuity.
‘2’ I
METHODS
I
Subjects
The subjects were two adult, female macaque monkeys (Macaca nemestrina). They had free access to Purina monkey chow, supplemented regularly with fresh fruit, and they were water deprived 5 days each week for approximately 20 hr before threshold testing. All thresholds were measured monocularly for the right eye of each subject during controlled fixation. Neither monkey was more than 0.5D myopic in its right eye. After initial training on the procedure described below, each monkey was anesthetized with isoflurane and a scleral search coil implanted in the right eye (so that eye position could be monitored) and a stainless steel sleeve attached to the skull (so that the head could be immobilize) (Judge et al., 1980). The fixation target, a red spot from a HeNe laser, was initially placed on the test grating and then gradually moved away over several sessions. Apparatus and procedure
The monkeys were seated in an acrylic chair facing a high resolution display oscilloscope (Tektronix 606 with P-31 phosphor). The mean luminance of the display was maintained at 16 cd/m* and it was viewed through a circular aperture (dimensions below) in an unilluminated white surround. A dim red fixation spot was presented on the surround to control the location of fixation relative to the test grating (Fig. 1). Acuity was tested with an orientation discrimination rather than a detection paradigm to minimize the use of cues to grating presence produced by stimuli beyond the resolution limit. Test stimuli were vertical or horizontal sinusoidal gratings of 0.55 Michelson contrast (L,, - ~~i”f~~~~+ Lma), presented with a smoothed onset (l/2 cycle of a raised cosine of 0.5 Hz). Each trial began, after a four second intertrial interval, with presentation of the dim
/
iI73 “II
i
Fig. 1. Schematic of the test procedure. The seated monkey monocularly viewed a red fixation spot (F), located at the testing eccentricity (0) from the nearest edge of the grating stimulus (S). The monkey’s head was fixed in place (H) and fixation was monitored with a scleral search coil.
red fixation spot. When the monkey fixated within an electronic window extending approx. f0.33 deg from the fixation spot, a 4500 Hz tone was presented and stimulus onset was initiated, The tone remained on for 1.8 see, and then went off, signalling the o~rtunjty to respond. The stimulus was present until either a response was made or the monkey’s fixation moved outside of the electronic window. Responses to the left button on the response panel were correct when the stimulus was a vertical grating, and to the right pushbutton when a horizontal grating was present. Correct choices were rewarded with fruit juice, while errors-were followed by presentation of a 6 set buzzing tone. If the monkey moved its fixation locus outside the window before responding, or responded on a pushbutton during the tone, the stimulus was removed and the tone extinguished, and after a 3 set beeping tone the intertrial interval was restarted. The spatial frequency of the test grating was varied according to a staircase, decreasing by one step (0.3 octave) after each error, and increasing, with probability 0.33, after each correct choice. Daily sessions consisted of 200 trials, and acuity thresholds were taken at 75% correct responding either by linear interpolation, or from probit fits to the daily psychometric functions (Finney, 1971). Acuity was tested monocularly along the horizontal meridian of the right eye in monkey 676, and along the superior and temporal meridia in monkey 675. Measurements were
Spatial resolution across macaque retina
made at eccentricities of 0, 3, 6, 12, 20, and in some cases 25 or 30deg (visual subtense of the fixation spot from the nearest edge of the stimulus). The test target was 185 cm from the observer for eccentricities of 0,3, and 6 deg and 93 cm for eccentricities beyond 6 deg. Diameter of the stimulus was 0.5 deg for 0 deg eccentricity, 1 deg for 3 and 6 deg eccentricity, 1.5 deg for 12 deg, and 3 deg for 20, 25 and 30 deg eccentricity. Thus, the stimulus was always approximately 20 cycles of a just resolvable grating. RESULTS
Figure 2 illustrates representative psychometric functions for monkey 676 for acuity measures along the horizontal nasal field meridian. The data points of each psychometric function are fitted by probit curves (Finney, 1971). It can be seen that threshold spatial frequency (taken as the intersection of the probit function with 75% correct identification) decreased in an orderly fashion with eccentricity from the fovea, but that the form of the psychometric function did not change with eccentricity. Mean acuity thresholds ( f SE) for monkey 676 along the horizontal meridian of the right eye are shown in Fig. 3, and for monkey 675 along the temporal and superior meridia of the right eye in Fig. 4. The dotted curve in each figure represents the Nyquist frequency calculated for cone density in the rhesus monkey retina (Perry & Cowey, 1985). Dashed lines indicate Nyquist frequencies calculated for On or Off P type ganglion cell density in the rhesus monkey retina (Perry & Cowey, 1985). Calcu1
9x7
30
30
0
E~ntfici~
(degf
Fig. 3. Mean acuity thresholds ( f SE) for monkey 676 along the horizontal meridian of the right eye. The dotted curve represents the average Nyquist frequency for cone density along the horizontal meridian of the rhesus monkey retina (Perry & Cowey, 1985). Dashed lines indicate average Nyquist frequencies calculated for the density of On or Off P ganglion cells along the horizontal meridian of the rhesus monkey retina (Perry et al., 1984).
lation of the Nyquist frequency is described in the Discussion. Measured acuities are in close agreement with Nyquist frequencies calculated for cone density out to eccentricities of about 10 deg, and with the Nyquist frequency calculated for ganglion cell density beyond 10 deg. DISCUSSION
This study demonstrates that macaque acuity, like that of humans, decreases very sharply with distance from the fovea, and that it is both quantitatively and qualitatively similar to that of humans. The decline in macaque acuity with distance from the fovea is steeper along nasal and superior visual field meridia than along the temporal visual field. Measured acuities closely matched cone Nyquist frequencies out to an eccentricity of approximately 10 deg, but matched the Nyquist frequency for On or Off P
4oc. 5 SpEdOFmque”cy
(c/&ig;o
Fig. 2. Representative psychometric functions for the spatial resolution of monkey 676 along the temporal visual field meridian. Squares (0 deg ~nt~~ty), circles (3 deg eccentricity), triangles (12 deg eccentricity), diamonds (20 deg eccentricity). Probit functions were fit to the data for each eccentricity. Thresholds were taken as the value corresponding to 75% correct. indicated by the dashed line.
0
30
0
30
Eccentricity (deg) Fig. 4. Mean acuity (&SE) for monkey 675 along the superior and temporal field meridia of the right eye. Theoretical curves are as in Fig. 3.
YXP
WILLIAM i-1. MEKIGANand LAURENCEM. KATZ
ganglion cells at greater eccentricities. These results imply that the major limitations on primate spatial vision may already be present in the retina, in the form of limitations on spatial
sampling of the visual image. In the central retina this limit is related to cone sampling density. and in peripheral retina to ganglion cell sampling density. The match between Nyquist frequency and resolution thresholds indicates that no further loss in resolution takes place beyond the retina, as might be expected if convergence or spatial averaging of neuronal signals in central visual pathways further limited acuity. Relation of macaque to human visual acuity The anatomy of the eye and retina are very similar in human and macque. The human eye is slightly larger, approximately 24 mm in length compared to about 20mm for the macaque (Rolls & Cowey, 1970). The larger eye results in a slightly greater retinal magnification factor (relation of mm of retinal extent to degrees of visual angle) in the human [0.291 mm/deg, Perry et al. (1984)] compared to the rhesus macaque [0.223 mm/deg, Perry et al. (1985)]. Cone density as a function of eccentricity is very similar in the rhesus monkey (Perry & Cowey, 1985), pigtailed monkey (Packer, Hendrickson & Curcio, 1989b), and in humans (Curcio et al., 1987) for eccentricities outside the fovea. However, cone density measurements for the fovea are quite variable from study to study. For example, Perry and Cowey (I 985) reported average fovea1 cone densities for the rhesus monkey of 140,500, while Packer et al. (1989b) found a mean of 210,O~ cones/mm2 in the pigtailed macaque. Much of the difference between these results appears to be due to the larger averaging area (90 x 90 u) used by Perry and Cowey than that used by Packer et al. (37 x 54 u). On the other hand, there do appear to be substantial differences in foveal cone density even between individuals from the same study. Curcio et al. (1987) found a 2.9-fold range around a mean fovea1 density of 161,900 cones/mm2 in a sample of four human retinas. Packer, Williams, Sekiguchi, Coletta and Galvin (1989a) reported a 1.4-fold range around a mean fovea1 cone density of 2 10,000 cones/mm’ in a sample of three pigtailed macaque retinas. It should be noted that because of the greater retinal magnification factor in humans, the mean cone density per degree of visual angle in the above studies was slightly higher in humans
than macaques. Thus, the human and macaque retinas are very similar, although the human retina has a slightly higher angular density of fovea1 cones. Human and macaque acuity were comparable in the present study, a result that confirms numerous studies of spatial vision in primates. Perhaps the most detailed cross-species comparison of acuity was that of Cavonius and Robbins (1973) who measured the acuity of macaques and humans over an 8 log unit range of luminances, using Landolt rings as test targets. They found that human and macaque acuity were very similar over a 4 log unit range of luminances, but that humans reached slightly higher acuity at the highest luminances, while macaques had superior acuity at the lowest tested luminances. The reported differences at high luminances were small (about 36%) and appear to be within the range of inter-individual differences found for central cone density. The spatial contrast sensitivity of adult macaques is also virtually identical to that of humans tested under the same conditions (DeValois, Morgan & Snodderly, 1974; Merigan, 1989). Thus, the anatomy and spatial resolution of the macaque eye are sufficiently like that of humans that an analysis, in macaques, of what limits acuity is likely to be directly applicable to human vision. Optical and luminance limits on visual acuity Central visual acuity in humans is limited to about 60 c/deg by optical degradation (Campbell & Green, 1965; Cambell & Gubisch, 1966), approximately the same limit imposed by the sampling density of photoreceptors (Williams, 1985). With eccentricity from the fovea, optical degradation of the visual image has been reported to decline more slowly than visual resolution (Jennings & Charman, 1981). Thus, optical quality appears not to limit the peripheral spatial resolution of humans, and the same is likely to be true for macaques. Spatial resolution is also limited by quanta1 fluctuations in the stimulus (Banks, Geisler & Bennett, 1987). Contrast thresholds decrease in proportion to the square root of luminance (Rose, 1942), resulting in a marked drop in spatial resolution. Because of this relationship, stimulus luminance and contrast must be reasonably high if acuity is to be limited primarily by retinal sampling density. In the present study, the stimulus luminance (16 cd/m’) was sufficiently high that macaque acuity is
Spatial resolution across macaque retina
nearly asymptotic at this luminance (Cavonius & Robbins, 1975). Sampling density limits on visual acuity
According to the sampling theorem, spatial resolution in one dimension is limited by sampling density such that the highest frequency that can be unambiguously imaged (the Nyquist frequency) is half the frequency of the array of detectors (Bracewell, 1975). For twodimensional arrays with hexagonal packing of receptors, the Nyquist frequency is F nyq = (0.5)(0.223)(1.15470)1/2
where D is receptor density per square mm, 0.223 is the conversion from mm of macaque retina to degrees of visual angle, and 1.1547 is the correction for hexagonal packing (Snyder & Miller, 1977). Because the Nyquist frequency represents a theoretical boundary for the veridical representation of an image, it is probably an important limit for such visual functions as recognizing objects or reading text, where ambiguity about stimulus interpretation would seriously degrade visual performance. On the other hand, it is clear that under some circumstances vertical-horizontal discrimination of grating orientation can be done at spatial frequencies beyond the Nyquist limit. For example, it was demonstrated by Williams and Coletta (1987) that human observers could discriminate the orientation of gratings up to spatial frequencies approximately 1.5 times the nominal Nyquist frequencies. More recently, Packer et al. (1989b) showed that separate stimulation of long or middle wavelength cones, which greatly reduces the average Nyquist frequency, did not decrease visual acuity. However, resolution beyond the Nyquist frequency was not apparent in the present study, in which Nyquist frequency was calculated from published counts of ganglion cells density (Perry et al., 1984) in which the extrafoveal displacement of ganglion cells was not taken into account. Ganglion cell density may be adjusted in later studies (e.g. Wassle, Grunert, Rohrenbeck & Boycott, 1989) by using the length of fibers of Henle (Schein, 1988; Perry & Cowey, 1988) to estimate ganglion cell displacement, but such an adjustment will have little effect on the calculation of Nyquist limits for ganglion cells. At eccentricities beyond 10 deg, measured visual acuity in this and previous studies (e.g. Wertheim, 1894) falls well below the Nyquist frequency calculated for cone photoreceptors.
989
Since ganglion cells are less numerous than cones beyond 10 deg eccentricity, we compared acuities beyond 10 deg to the Nyquist calculated for P type retinal ganglion cells (which make up about 80% of ganglion cells (Perry et al., 1984). We considered On and Off ganglion cell matrices independent, on the basis of the calculation (Schein & DeMonasterio, 1987; Wassle, 1989) that there are somewhat over two ganglion cells for each central cone in the primate, and, thus, that On and Off ganglion cells may receive independent input from each cone. It can be seen in Figs 3 and 4 that acuity beyond 10 degrees agrees well with predictions from the Nyquist frequency for On or Off P ganglion cells [also see Thibos et al. (1987b)], and that meridional differences in ganglion cell density are reflected in different acuities. Since M ganglion cells make up only about 10% of retinal ganglion cells (Perry et al., 1984) the Nyquist frequency for the matrix of On or Off M cells would be lower by approximately 3 fold than that calculated here for P cells. While such a matrix could subserve many visual capacities, it is unlikely that it could mediate tasks requiring the visibility of high spatial frequencies, such as reading small text at a distance. Spatial averaging and the resolution limit
Spatial resolution can also be limited by spatial averaging across the aperture of neural elements (Snyder & Miller, 1977; Barlow, 1981). It is already clear from the data of Figs 3 and 4 that spatial averaging could not uniquely limit primate visual resolution, since there appear to be no further constraints on acuity beyond those due to retinal sampling density. However, it is possible that acuity might be jointly limited by sampling density and spatial averaging. Averaging cannot limit resolution when the summation aperture is small relative to the spacing of neural detectors. This is the case for photoreceptors in the monkey retina, whose aperture is shown by the data of Thibos et al. (1987a) to limit detection to about 130 c/deg in the fovea, and about 45 c/deg at 20 deg eccentricity. This is probably also true for P ganglion cells in the central retina, since their receptive field centers appear to be driven by single cones (Shapley & Perry, 1987). However, larger summation areas resulting from convergence can limit spatial resolution because of either the reduced sampling density of the matrix of second level neurons, or their greater receptive
990
WILLIAM H. MERIGAN
field areas (which produces lower resolution in those cells with linear spatial summation). Receptive field size in the cat retina has been shown to be well predicted by the dendritic field size of retinal ganglion cells (Peichl & Wassle, 1983). It would be most useful if such a relationship were also known for the primate retina, because excellent data are available for retinal ganglion cell dendritic fields in both macaque (Perry et al., 1984), and human (Rodieck et al., 1985). These data indicate, among other things, that the dendritic fields of M ganglion cells (which project to magnocellular layers of the lateral geniculate) are about 3 times greater in diameter than those of P ganglion cells (which project to parvocellular layers of the geniculate). Unfortunately, the relation of dendritic to receptive field size is not known for the primate, and, thus, this anatomical data cannot be used to calculate limits on acuity. The most direct way to determine the effects of spatial averaging in the primate visual pathway is to measure the spatial resolution of single cells, or, in the case of linearly summating cells, the size of the receptive field center. One should bear in mind that since such measures do not reflect sampling density, they cannot be used to infer the resolution of visual pathways. Crook et al. (1988) report such data for retinal ganglion cells of the macaque. They found that the aperture limitation on resolution in P cells was only slightly below the psychophysical resolution measured in the present study. A similar result has been found in the macaque lateral geniculate nucleus by Kaplan and Shapley (1982), Hicks et al. (1983), Derrington and Lennie (1984) Blakemore and VitalDurand (1986), and in macaque striate cortex by Hawken and Parker (1986) and Blakemore and Vital-Durand (1983). Unfortunately, the basis of the spatial averaging implied by the size of receptive field centers or the resolution of single neurons remains unclear. If central macaque P cells actually receive input to their receptive field centers from single cones (Shapley & Perry, 1986), receptive field centers should be much smaller than reported in the above studies, and resolution much higher. The apparently large receptive field centers for central P cells reported in these studies probably reflect a joint effect of optical degradation and eye movements. On the other hand, the reported center size for M cells and more peripheral P cells may be correct since they likely receive input from multiple cones, and
and
LAURENCE M. KATZ
optical and eye movement artifacts are less likely to have affected these measurements. The agreement between measured or calculated resolution for such cells is reasonably close to the psychophysical acuity measured in this study. This agreement suggests that spatial resolution in the macaque may be partially limited by spatial averaging over the receptive field, in addition to the previously described sampling density limitations. Ackno~vledgemenu-We
thank Cheryl Ruff-Neri for assistance in testing monkeys and Beverley Katz for serving as an observer in this experiment. Drs William Newsome and Robert Wurtz provided instruction on the technique of eye coil placement, and Drs Tatiana Pasternak and David R. Williams commented on the manuscript. This research was supported by grants NSF 8518858, ES01247, EY01319 and AFOSR 89-004 I
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