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Vernier acuity in the cat: Its relation to hyperacuity
vlrion &s. Vol. 26. No. 8, pp. 1?63-1271. Printed in Great Bntain
86 53.00 + 0.00 W?-6989 Pergamon Journals Ltd
1986
VERNIER ACUITY IN THE CAT: ITS RELATION TO HYPERACUITY SYLVIE BELLEVILLE* and FRANC=
WILKIXSOE:
Department of Psychology, McGill University, Montreal, Quebec, Canada H3A IBl (Receked
5 August 198.5;in revised form 4 February
1986)
Abstract-Vernier thresholds were measured behaviourally in tive cats using offsets in gratings of two spatial frequencies and in singIe tines. Thresholds ranged from 2.2 to 6.7’. and no threshold differences were found across stimuli. These results are discussed in relationships with published spatial resolution data and are related to the optical and neural characteristics of the cat’s visual system. It is concluded that if vernier acuity is a hyperacuity in cats, the improvement in grain is not of the same magnitude as it is in humans. Cats
Vernier acuity
Spatial resolution
Hyperacuity
of neurons in the input layer IV of striate cortex as a possible substrate for this reconstruction. The remarkable sensitivity of human subjects in Striate cortex has been implicated in vernier detecting vernier offsets has been recognized for offset detection in the only published work to almost a century (I-Iering, 1899). Under optima1 date which has examined this ability in a nonconditions humans can detect vernier offsetsdf human species-the cat (Berkley and Sprague, as httle as 4” of arc, an order of magnitude 1979; Sprague et al., 1979). Only one of three smaller than the minima1 intercone distance destriate cats was able to distinguish between (Polyak, I94 1). Westheimer (1975) grouped single lines with and without offsets, and this under the label “hyperacuity” several spatial animal’s vernier acuity was 12 times worse than abilities having a similarly fine grain. Several its preoperative threshold. In a more recent hypotheses have been put forward recently report, Berkley and Bush (1984) describe which attempt to explain how such sensitivity modest threshold impairments as a consequence may come about (Westheimer and McKee, of pe~endicuIar slicing through the striate 1977a, b; Barlow, 1979, I98 1; Westheimer, cortex. 1979, 198 I; Crick et ai., 198I; Fable and Poggio, Vernier acuity in intact cats was reported by 1981; Watt, 1984; Zucker and Hummel, In these investigators to range from 4 to 8’. In press). To date, few efforts have been made to contrast to human vernier acuity, this threshold translate these hypotheses into concrete neural does not exceed the limit set by the cone mosaic models. However, two general types of neural (Steinberg et al., 1973) nor is it better than the coding have been suggested. Westheimer threshofd for grating resolution in cats (Blake and McKee (1977a, b; Westheimer, 1979, 1981) et al., 1974; Mitchell et al., 1977). This might favour a modular approach to visual processing suggest that no speciai interpolation process is in which relative positions of stimuli within a necessary to extract offset information in the local area are evaluated separately from other cat visual system. However, the task used by characteristics of the stimuli. Barlow (1979, Berkley and Sprague (offset in a small line 1981), on the other hand, suggests that hyper- segment), while comparable to that used in acuity is provided by a fine-grained recon- human studies, may have lacked the salience struction of the retinal image which is imple- necessary to elicit optima! performance from mented at an early stage of cortical processing cats. For this reason, we have undertaken and provides the basis for later stages of feature a more extensive examination of vernier analysis. Barlow points to the very high density thresholds in cats. In the present study, we report measurements of vernier acuity made in visually intact cats using offsets in two sets of *Address correspondence to: S. Belleville, Dept. of Psycholhigh contrast square wave gratings of different ogy, 1205 Dr. Penfield Ave., Montreal, Quebec, Canada, spatial frequency. We also report vernier H3A IBI. INTRODUCTION
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SYLVIE BELLEWLLEand FRASCES WILKINSON
thresholds measured using offsets in a set of single line stimuli.
locked. If an animal responded appropriately, it was reinforced with a preferred food (beef baby food); if however it jumped to the incorrect METHOD stimulus, the trap door opened and the cat fell a distance of 12 inches onto a soft surface. This Subjects reinforcement procedure was maintained during The subjects were five cats born and raised in both initial training and threshold measureour laboratory. Three of these were littermates ment. Our prior experience with the apparatus (MK78, MK79, and MK80). The cats were showed that if the animal was permitted to individually housed and were provided with delay in responding, its attention was distracted water and dry cat food ad iibitum. At the onset by other aspects of the apparatus. Conof threshold measurement, the cats ranged in sequently, the animals were allowed an initial age from 4 to 8 months (see Table 1). 30sec period to respond and were then gently prodded at regular intervals using a flat wooden Apparafus plunger which fits snuggly into the tunnel The animals were tested on a jumping stand behind the cat. The left-right position of the similar to that described by Mitchell et al. stimuli was varied randomly. After every trial, (1976). They were trained to jump from an the stimuli were systematically moved in order enclosed platform onto one of two stimuli which to keep constant any auditory cues. lay on Iockable trap doors. The height of the During the learning phase, the height of the jumping platform was adjustable. The walls of jumping platform was gradually increased from the jumping platform were flared so that the an initial level of 30cm to a final height of experimenter, positioned behind the animal, approximately 50 cm which then remained concould not see which stimulus the animal was stant throughout threshold evaluation (see looking at (latera head movem~ts~but could below). Thus, the viewing distance was always see if the animal was leaning below the floor of kept at or beyond the near points of accommothe platform. dation for cats as measured by Bloom and Berkley (1977). During the initial learning Stimuli period, we were very careful to prevent the Three stimulus sets were used: high contrast animal from attempting to lean toward the gratings of two spatial frequency (grating 1: stimuli before jumping. Cats that showed a 0.4 c/deg; grating 2: 1.1 c/deg) and single lines tendency to lean were discouraged by placing (21” long, 16’ wide). All stimuli were computer the experimenter’s hand just below the tunnel generated on a laser printer with a spatial exit. resolution of l/300 in. A series of offsets were We monitored viewing distance on a frequent produced, the sizes of which ranged from 49.5 basis throughout training and threshold delinto 1.1 minutes of visual angle (19 offset sizes per eation. In addition to the distance monitoring set). The grating stimuli subtended a total area done by the experimenters, some of the testing of 27” by 21”; grating 1 stimuli contained 13 sessions were videotaped. The position of the cyctes and grating 2 stimuli contained 29 cycles. animal’s eyes just prior to its jump was used as In the preceding description, visual angles are its viewing distance. We consider this as a based on a viewing distance of 50 cm since most conservative estimate as the animal may actuof our estimates were done from this distance ally make its choice from a greater distance (see below). The positive stimulus was a grating during its approach toward the edge of the or a single line with a horizontal offset at the jumping platform. The learning criterion was set to 90% correct midpoint of each line. The negative stimulus was an identical grating or single line without performance on 30 consecutive trials. Since the offset. The average luminance level measured at vernier task is highly learning dependent in the stimufi was 305 cd/m’. human adults (Westheimer and Hauske, 1975), the animals were given a large number of pracTraining procedure tice trials on various offset sizes after reaching As a first step, the animals were trained to criterion and before the measurement of their discriminate a grating with a large offset from a vernier thresholds. After completion of testing grating with no offset in 40 trial daily sessions. on any one of the three stimulus sets, the The door bearing the positive stimulus was animals were transferred to the next stimulus
Cat vernier acuity
(for which a criterion of 27130 correct responses was required), and were again given practice trials before their thresholds were measured. Threshold measurements
Two psychophysical procedures were employed to delineate the thresholds of our animals. Viewing distance remained constant throughout the threshold evaluation and was 50cm for all cats except for MK58 whose viewing distance was 47 cm. Modified staircase procedure. Within a 40-trial daily session the stimuli were presented in order of decreasing offset until the animal failed to respond correctly. A failure produced an increase of four steps in the offset series (66’ at 50 cm). This increase was followed by the presentation of the next stimulus in decreasing order of offset until the animal failed again. This was continued over the 40 trials. Animals were tested over a sufficient number of days to gather 50 to 130 trials at each near-threshold value. Method of constant stimuli. From the performance of the animal on the practice trials and from previous data from other anin&_lO offset values were chosen which were expected to bracket the threshold. These 10 offset values were presented in a random order. Four sets of 10 random presentations were given every day over a period of 20 days totalling 80 trials at each offset value. One cat (MK58) was tested using both psychophysical procedures but a single stimulus set (grating 1). The other four cats were tested on all three stimulus sets using a single psychophysical procedure (MK68: method of constant stimuli; MK78, MK79, and MK80: staircase procedure). All four were tested first with grating 1. Two cats, MK68 and MK78, were then tested according to the following sequence: grating 2, single line. The sequence was reversed for MK79 and MK80: single line, grating 2. Following this sequence, MK80’s threshold on grating 1 was retested at the original height
1265
(50 cm) and at a higher position
(75 cm). Assuming that we correctly estimated the position of the animal’s eyes in the first measure of the threshold, testing the animal from an increased distance should produce similar results. Table 1 indicates the psychophysical procedure used, as well as the order of testing on each stimulus for the five animals.
RESULTS
Table 1 shows the number of trials required to reach criterion for each of our subjects (range: 433-266 1). The variation observed in the number of trials required to learn the task may reflect individual differences or differences due to age at onset of testing. While the issue of age is an important one, and one which we are currently investigating, it will not be considered further in the present report because all our threshold measurements were made after 4 months of age and no age-related threshold differences were found (see below). Thresholds
The performance of each subject was plotted against offset size on a linear scale separately for each stimulus and/or measurement condition. Threshold was determined by fitting a straight line to each data set with regression analysis and by taking the offset value corresponding to the estimated 70% correct performance. We included in the regression analysis only the data points in the descending portion of the psychometric curve. In classifying data points as belonging to the descending portion we used the following criteria. Upper limit. Based on performance on the four largest offset values, we determined a confidence interval (2 SD) for asymptotic performance. The smallest offset value for which performance still fell within this range was taken as the top of the curve.
Table I. Training and testing histories for the five cats Cat
Age (days) at onset of training Trials to criterion Age (months) at threshold measurement Psychophysical procedure Stimulus order
MKSS
MK6S
MK7S
92 -925 s-10 SP_and a Gl
45 2661 7-9 cs GI-G2-SL
65 1042 4-6 SP GI-G2-SL
MK79 65 582 4-6 SP GI-SL-G2
MKSO 150 433 6-8 SP GI-SL-GZ-GI-GI’
‘This animal was retested on grating 1 from two different viewing distances (50 and 75 cm). CS: methodof constant stimuli; SP: staircase procedure; G I: grating 1 (0.4 c/deg); G2: grating 2 (1.1c/deg); SL: single line.
I266
SYLLIE BELLEVILLEand
When retested on grating 1, MK80 was found to have thresholds of 3.4’ and 3.6’ at the original viewing distance and at 75 cm respectivefy. These two values are very similar; they are also very close to MK80’s performance in the first testing on grating I (3.3’).
1X
DISCUSSION
The vernier task proved difficult for cats to learn, but when they had acquired it, they performed at a very high level with large offsets 2 4 6 a 10 12 14 16 and showed rapid falloff to chance performance Offset (min of arc) at small offset values, The offset thresholds measured in the five cats were found to range from 2.2’ to 6.7’. This range is not due to the use 100 of two different psychophysical procedures (staircase and constant stimuli) because the two 90 procedures when used in the same cat (MK58) . . 80 . yielded similar threshold values: 6.7 and 6.4’ for z . grating 1 (see Table 2). Since the role of practice ---__---___-__---y 70 8 u in achieving optimal vernier performance has . 8 60 Constant stimuli been emphasized in the human literature (WestMK58 . /-= heimer and Hauske, 1975) it is important to 50 note that all threshold values were determined -* 40 following extensive over-training on various ~, ,, , , , , , offset sizes. Furthermore, we did not find any 2 4 6 a 10 12 14 16 significant improvement as a function of Offset (mln of arc) presentation order, which might have been exFig. I. Frequency of seeing curves and fitted lines for MKS8 pected if the cats were not performing optimally tested on grating I using the staircase procedure (top) and on the earty tasks. Consequently, it is very the method of constant stimuli (bottom). probable that the thresholds we measured reflect the best performance of which our animals were Lotser hit. The smallest offset included was capable under the particular test conditions the largest offset for which performance did used. This conclusion receives further strong not differ significantly from chance (normal support from the data of MK80. This cat was approximation to the binomial distribution). The first cat, MK58, was tested using both the Table 2. Vernier acuity thresholds (70% cutoff criterion) for MK58 (a) and for MK68, MK78, MK79, MK80 (b). A staircase and the method of constant stimuli on second threshold estimate is given in brackets grating I. Figure 1 shows the frequency of MK58 seeing curves and the fitted lines for the two data sets. The estimated thresholds for this Staircase Constant stimuli (4 animal were 6.4 and 6.7’ on the staircase and Grating I constant stimuli respectively (Table 2a). The 70% threshold 6.4’ (4.2’) four remaining cats were tested on the three (60% cutoff) stimulus sets. Their frequency of seeing curves MK80 MK78 MK79 MK68 (b) and regression lines are shown in Fig. 2. The Grating -1 thresholds measured on all three stimuli ranged 3.3. 5.0 5.4 3.3‘ threshold from 2.2 to 6.1’ (Table 2b). As can be seen from 70% (2.7’) (4.1’) (2.6’) (4.2’) (60% cutoff) Table 2b, this overall range is quite representaGrating 2 tive of the range of values measured on each of 70% threshold 2.6’ 3.3’ 4.3’ 2.2’ (1.9’) (2.7’) the three stimulus patterns. The mean thresh- (60% cutoff) (1.6’) (3.6’) olds for each stimulus set are 4.7;iSDS 1.4) for Single line 4.6 3.1’ 6.1’ 3.3 grating 1, 3.I’(SD = 0.9) for grating 2, and 4.3’ 70% threshold (2.3’) (3.9’) (1.4’) (5.0’) (60% cutoff) (SD = 1.4) for the single line. 40
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retested on grating 1 at two different heights following completion of the grating l-grating 2-single line sequence, and showed thresholds almost identical to its initial threshold on grating 1 at both heights (3.4 and 3.6’ vs 3.39. The finding of identical thresholds at 50 and 75 cm is additional strong evidence that our viewing distance estimates were quite accurate.
One of the questions which motivated this study was whether thresholds in the hyperacuity range could be obtained on the vernier task if a more salient stimulus than the single line target of previous studies were employed. We thought the redundant nature of our grating stimuli might increase their salience. The issue of hyperacuity will be considered at length below; first,
1268
SYLLIE BELLEYILLEand FRASCES WILKISSOU
however, our findings must be compared directly with those of Berkley and Sprague (1979). Our cats did not show consistently better thresholds on the grating stimuli (grating 1 and grating 2) than on our single line stimulus, indicating that under our conditions, gratings and single lines are equally effective vernier targets. The thresholds reported by Berkley and Sprague (1979) and more recently by Berkley and Bush (1982) (4-8’) overlap the upper end of our range. It should be noted, however, that we have used a more conservative estimate of threshold (70% vs 56% correct). Since most of the behavioural studies of grating acuity to which we wish to compare our results (see below) use a 70% or 75% cutoff, this seemed the more appropriate choice. Berkley and Sprague’s cats maintained 70% performance at offset values of about 10’ of arc. Applying a less conservative cutoff criterion (60%) to our data yields threshold estimates that range from 1.4 to 5’ (see Table 2). Thus it would seem that our stimulus configuration supports somewhat better vernier offset detection. Although we found no difference between grating aiid Ogle line stimuli, it is possible that all our stimuli were more salient because they covered a much larger portion of the visual field than the 5’ segment line of the previous studies. In all cases, of course, the only relevant information is located within a very small region at the line centre. It should also be noted that the average luminance was at least I log unit higher in the present study. However, we doubt that luminance level is the critical factor because estimates of spatial acuity made under similar luminance conditions in our laboratory (Wilkinson and Belleville, unpublished observations) are not better than the ones reported by Berkley and Sprague (1979). We have recently learned that Mitchell and Murphy (personal communication) have obtained vernier thresholds of l-2’ of arc using the temporally displaced offset procedure introduced by Shimojo ef al. (1984) for human infants. Whether the detection of dynamic and static offsets reflects the same neural mechanism remains to be determined. Hyperacuity
The ability to detect vernier offsets has been termed a hyperacuity in humans because its threshold is considerably better than the spatial resolution of the system as determined by grating acuity or other spatial resolution measures.
Because of the efficient sampling strategy of the human visual system, spatial acuity approaches very closely the resolution limit imposed by diffraction in the human optical system (Krauskopf. 1962; Westheimer and Campbell, 1962). In the case of resolution acuity, the highly regular cone mosaic is fully exploited. Yet vernier exceeds this limit by an order of magnitude. Sampling at discrete points provides the information necessary to reconstruct the retinal image through interpolation (Barlow, 1981; Westheimer, 1979, 1981; Hirsch and Hylton, 1984: Snyder, 1982). Hirsch and Hylton (1984) have recently argued that the highly ordered hexagonal mosaic in the primate fovea provides the metric from which relative location in space can be determined even to accuracies in the hyperacuity range. It is widely assumed that the interpolation is caried out at the cortical level, and several authors (Barlow, 1979, 1981; Crick et al., 1980; Fahle and Poggio, 1983) have specifically pointed to layer IVC, a major target of the parvocellular geniculate laminae as a likely substrate. In primates, the cells in this layer have the same general receptive field structure as retinal ganglion and geniculate cells (Hubel and Wiesel, 1968, 1977; Blasdel and Fitzpatrick, 1984) but are much more numerous (O’Kusky and Colonnier, 1982). Hence they could serve to provide a very finegrained reconstruction of the information encoded by the retinal X-cells. Hyperacuity
in cats.?
In human subjects, behaviourally assessed spatial acuity coincides closely with the resoiution limit set by optical transmission and the cone mosaic, and hyperacuities are defined relative to this common limit. In cats, however, these three factors do not coincide so closely. Optical resolving power varies with pupil size (Robson and Enroth-Cugell, 1974; EnrothCugell and Robson, 1978; Woodhouse and Campbell, 1979) but under optimal conditions, values as high as 20 c/deg have been reported (Enroth-Cugell and Robson, 1978). Minimum intercone distance in region of peak cone density (area centralis) has been reported by Steinberg et al. (1973) to be 1.7’. If the cone mosaic set the limit for spatial resolution, one would predict a cutoff spatial frequency in the neighbourhood of 16 c/deg (exact value would depend on the nature of and degree of regularity in the mosaic). However, behavioural measures of cutoff spatial frequency for high contrast
Cat vernier acuity
gratings place the limit considerably below either the optical or the receptor limit (see below). It appears that the resolution of the cone mosaic is lost at the ganglion cell level, where even in the area centralis a considerable degree of convergence occurs (Stone, 1965; Steinberg er al., 1973; Hughes, 1975). Interpretation of ganglion cell densities is somewhat complicated by the fact that several classes of ganglion cell have been distinguished on the basis of their morphological and spatiotemporal response properties (reviewed by Stone, 1983), and at least two of these (alpha or Y cells and beta or X cells) can be further subdivided into off-centre and on-centre groups, The beta (X) cells show the highest spatial resolution (Cleland et al., 1979) and woutd hence be presumed to be important for detection of vernier offsets (Crick et al., 1981; Berkley and Bush, 1983; Zucker and Hummel, In press). On and off beta cells appear to form independent grids of approximately equal density. There is also some suggestion that the positions of cell pairs from the two grids are highly correlated (Wassle et al., i 98 1) suggesfig that the same spatial location is SimultaneousIy sampled by two channels. This has been interpreted by a number of investigators (Barlow, 1981; Fahle and Poggio, 198 1; Wassle et al., 1981) as indicating that the task of signalling intensity relative to local background is split into two parts (greater than and lower than background). On this basis, the spatial resolution of the visual system woutd be determined by the minimum interganglion cell distance in one of the two maps, a distance which Wassle et al. (1981) calculate as subtending a visual angle of 5.4’ of arc. The assumption that on and off grids operate independently has been questioned by Hughes (198 1). In the sort of heterogeneous model he proposes, thresholds up to 10 c/deg co&d be supported. Thus anatomical considerations do not provide a clear estimate of the resolution of the information leaving the retina. The spatial resolution of the cat’s visual system has been assessed both behaviourally (Smith, 1936; Blake et al., 1974; Muir and ~itchell,l975; Jacobson et al., 1976; Mitchell et al., 1977; Pasternak and Merigan, 198-l; Elberger, 1982) and by evoked potentials (Berkley and Watkins, 1973; Campbell et gl., 1973; Harris, 1978) and values ranging from below 3 c/deg to over lOc/deg have been reported. The interactive role of several factors
1269
(luminance, total stimulus area, motivational conditions, threshold definition) in determining this range is not yet fully understood. Abasing (‘Williams and Collier, 1983; Yellott, 1983) must also be considered a possible contributing factor to the highest values reported. If we use one of the highest reported behavioural cutoffs (9c/deg) (Jacobson et al., 1976), an average cutoff (6 c/deg) (Blake et al., 1974), and one of the lowest under photopic conditions (3 c/deg) (Pasternak and Merigan, 1981) as examples, the best vernier acuity for which no special interpolation would be required woutd be 3.3, 5 and 10’ respectively. We have not tested spatial acuity in the cats used in this study; however, other cats tested in our laboratory under similar test procedures (including threshold criterion and lighting conditions) to those used for the vernier task routinely produce acuity cutoffs in the 4-4.5 c/deg range which applied to vernier threshold predicts a limit of about 7’ without interpolation. Thus based on spatial acuity measurements, one must conclude that if the cat’s vernier acuity is in the hyperacuity range the interpolated representation provides an improvement in grain of not greater than three times, much less than the order of magnitude differences seen in the human. It should be noted that stereoacuity thresholds in the cat show a spatial precision similar to that reported here for vernier detection (4-10 min of arc disparity) (Kaye et al., 1981; Timney, 1981, 1983, 1984). This observation is interesting because it indicates that two abilities which are in the hyperacuity range in humans are spatially limited to a similar extent in the cat. This is suggestive of a common neural substrate at an early stage of visual processing (Berry, 1948; Stigmar, 1970). That substrate is likeiy to involve the X-cellinput target cells in striate cortex (Berkley and Bush, 1984; Crick et at., 1981). As discussed above, the large numerical difference between geniculate input fibres and cortical cells in layer IVC/3 of primates has led to speculation about their involvement in the interpolation process. In the cat, the ratio of geniculate projection cells to area 17 target ceiis is certainly smalier than in the primate: Beaulieu and Colonnier (1983) estimate l/20 in cats (Layer IV) and l/55 in monkeys (Layer IVA and IVC). Another difference between cat and primate which may prove significant in this context is that the receptive field properties of the layer IV target cells which receive X-cell input are dissimilar.
SL LL IE BELLE~ILLE and FR;\.UCES WILI;IXOZ
1’70
As documented initially by Hubel and Wiesel (1968. 1977). and confirmed bv others (BIasdell and Fitzpatrick, 1984). the cells of layer IVC in the primate are monocularly activated and have nonoriented receptiv-e fields. In the cat. on the other hand. cells in layer IV which receive direct X-cell input are predominantly simple cells with elongated receptive fields (Bullier and Henry, 1979; Gilbert and Wiesel, 1979). The proportion of nonoriented cells in layer IV in the cat is much smaller than in the primate (Bullier and Henry, 1979, 1980). Perhaps these differences account for the modest degree of spatial interpolation which our data indicate in the cat. ,~cli,ton/erfgemeItts-We would like to thank Yvan Leclerc and Dr Steven Zucker for their help in producing the stimuli. This study was supported by NSERC grant No. 7551 to F.W.
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Elberger A. J. (1982) The corpus callosum is a critical factor for developing maximum visual acuity. ~ezf Bruin Res. 5. 350-353. Enroth-CugelI C. and Robson J. G. (1974) Direct measurement of image quality in the cat eye. J. Physiol., Land. 233, 3op-3 I p. Fable M. and Poggio T. (1981) Visual hyperacuity: spatiotemporal interpolation in human vision, Proc. R. Sec. B213, 451377. Gilbert C. D. and Wiesel T. N. (1979) ~Iorphology and intracortical projections of functionally characterised neurones in the cat visual cortex. :Varure, Lond. 280, 12O-125. Harris L. R. (1978) Contrast sensitivity and acuity of a conscious cat measured by the occipital evoked potential. Vision Res. 18, 175-178. Hering E. (1899) Uber die grenzen der sehschdrfe. Ber. ~~aih-ph~s. Cl. d. Konigl. Sachs. Geseli. Wiss. Leipzig: Naturwiss. Teii, pp. 1624. Hirsch J. and Hylton R. (1984) Quality of the primate photoreceptor lattice and limits of spatial vision. Vision Res. 24, 347-355. Hubel D. H. and Wiesel T. N. (1968) Receptive fields and functional architecture of monkey striate cortex, J. Physiol., Lond. 195, 215-343. Hubel D. H. and Wiesel T. N. (1977) Functional architecture of macaque monkey visual cortex. Froc. R. Sot. BI98, I-59. Hughes A. (1975) A quantitative analysis of the cat retinal ganglion cell topography. J. camp. Neurof. 163, 107-128. Hughes A. (1981) Cat retina and the sampling theorem; the relation of transient and sustained brisk-unit cut-off frequency to alpha and beta mode cell density. E.rp/ Bruin Res. 42, 196-202. Jacobson S. G., Franklin K. 8. J. and McDonald W. 1. M. (1976) Visual acuity of the cat. Yirion Res. 16, I1411143. Kaye IM., Mitchell D. E. and Cynader M (1981) Selective loss of binocular depth perception after ablation of cat visual cortex. Nature, Lond. 293, 6O-62. Krauskopf J. (1962) Light distribution in human retinal images. J. opt. Sot. Am. 52, 1046-1050. Mitchell D. E., Giffin F. and Ttmney 8. (1977) A behavioural technique for the rapid assessment of visual capabilities of kittens. Perceprion 6, 131-193. Mitchell D. E., GitTin F., Wilkinson F. E., Anderson P. and Smith M.-L. (1976) Visual resolution in young kittens. Vision Res. 16, 3633366. Muir D. W. and Mitchell D. E. (1975) Behavioral deficits in cats following early selected visual exposure to contours of a single orientation. Brain Res. 85, 459-477. O’Kusky J. and Colonnier M. (1982) A laminar analysis of the number of neurons, giia and synapses in the visual cortex (area 17) of adult macaque monkeys. J. camp. Neural. 210, 278-290. Pasternak T. and Merigan W. H. (1981) The luminance dependence of spatial vision in the cat. Vision Res. 21, 1333-1339. Polyak S. L. (1941) Chicago.
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Robson J. G. and Enroth-Cugell C. (1978) Light distribution in the cat-s retinal image. Vision Res. 18. 159-173. Shimojo S., Birch E. E., Gwiazda J. and Held R. (1984) Development of vernier acuity in infants. Vision Res. 24, 721-728. Smith K. U. (f936) Visual disc~mination in the cat: iv. The visual acuity of the cat in relation to stimulus distance. J. genet. Psycho/. 49, 297-313.
Snyder A. W. (1982) Hyperacuity and interpolation by the visual pathways. Vision Res. 22, 12 19-1220. Sprague J. M., Berkley M. A. and Hughes H. C. (1979) Visual acuity functions and pattern di~rimination in the desttiate cat. Acra neurobiol. e.rp. 39, 643-682. Steinberg R. H., Reid M. and Lacy P. L. (1973) The distribution of rods and cones in the retina of the cat (F&is damest~cas~. J. camp. Neural. 148, 229-248. Stigmar G. (1970) Observations on vernier and stereoacuity with special reference to their relationship. Rcra ophthal. 48, 979-997.
Stone J. (1965) A quantitative analysis of the distribution of ganglion cells in the cat’s retina. J. camp Neural. 124, 337-352. Stone J. (1983) Paraiiel Processing in the Visuaf System. Plenum Press. New York. Timney B. (1981) Development of binocular depth perception in kittens. Incesr. Ophrkal. visual Sci. 21, 493-496. Timney B. (1983) The effects of early and late monocular deprivation on binocular depth perception in cats. Decl Brain Res. 7, 235-243. Timney B. (1984) Monocu!ar deprivation and binocular depth perception in kittens. In Dewlopment of Visual Parhwys in ‘~fammais (Edited by Stone J., Dreher 8. and Rapaport D. H.), pp. 405-423. Liss, New York. Wassle I-I., Boycott F. R. S. and Illing R. B. (1981) Morphology and mosaic of on- and off-beta cells in the
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Westheimer G. and McKee S. P. (1977a) Integration regions for visual hyperacuity. Vision Res. 17, 89-93. Westheimer G. and McKee S. P. (I977b) Spatial con~guratioo for visual hypewcuity. Vison Res. 17, 94 l-947.
Williams D. R. and Collier R. (1983) Consequences of spatial sampting by a human protoreceptor mosaic. Science 221, 385-387.
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86 53.00 + 0.00 W?-6989 Pergamon Journals Ltd
1986
VERNIER ACUITY IN THE CAT: ITS RELATION TO HYPERACUITY SYLVIE BELLEVILLE* and FRANC=
WILKIXSOE:
Department of Psychology, McGill University, Montreal, Quebec, Canada H3A IBl (Receked
5 August 198.5;in revised form 4 February
1986)
Abstract-Vernier thresholds were measured behaviourally in tive cats using offsets in gratings of two spatial frequencies and in singIe tines. Thresholds ranged from 2.2 to 6.7’. and no threshold differences were found across stimuli. These results are discussed in relationships with published spatial resolution data and are related to the optical and neural characteristics of the cat’s visual system. It is concluded that if vernier acuity is a hyperacuity in cats, the improvement in grain is not of the same magnitude as it is in humans. Cats
Vernier acuity
Spatial resolution
Hyperacuity
of neurons in the input layer IV of striate cortex as a possible substrate for this reconstruction. The remarkable sensitivity of human subjects in Striate cortex has been implicated in vernier detecting vernier offsets has been recognized for offset detection in the only published work to almost a century (I-Iering, 1899). Under optima1 date which has examined this ability in a nonconditions humans can detect vernier offsetsdf human species-the cat (Berkley and Sprague, as httle as 4” of arc, an order of magnitude 1979; Sprague et al., 1979). Only one of three smaller than the minima1 intercone distance destriate cats was able to distinguish between (Polyak, I94 1). Westheimer (1975) grouped single lines with and without offsets, and this under the label “hyperacuity” several spatial animal’s vernier acuity was 12 times worse than abilities having a similarly fine grain. Several its preoperative threshold. In a more recent hypotheses have been put forward recently report, Berkley and Bush (1984) describe which attempt to explain how such sensitivity modest threshold impairments as a consequence may come about (Westheimer and McKee, of pe~endicuIar slicing through the striate 1977a, b; Barlow, 1979, I98 1; Westheimer, cortex. 1979, 198 I; Crick et ai., 198I; Fable and Poggio, Vernier acuity in intact cats was reported by 1981; Watt, 1984; Zucker and Hummel, In these investigators to range from 4 to 8’. In press). To date, few efforts have been made to contrast to human vernier acuity, this threshold translate these hypotheses into concrete neural does not exceed the limit set by the cone mosaic models. However, two general types of neural (Steinberg et al., 1973) nor is it better than the coding have been suggested. Westheimer threshofd for grating resolution in cats (Blake and McKee (1977a, b; Westheimer, 1979, 1981) et al., 1974; Mitchell et al., 1977). This might favour a modular approach to visual processing suggest that no speciai interpolation process is in which relative positions of stimuli within a necessary to extract offset information in the local area are evaluated separately from other cat visual system. However, the task used by characteristics of the stimuli. Barlow (1979, Berkley and Sprague (offset in a small line 1981), on the other hand, suggests that hyper- segment), while comparable to that used in acuity is provided by a fine-grained recon- human studies, may have lacked the salience struction of the retinal image which is imple- necessary to elicit optima! performance from mented at an early stage of cortical processing cats. For this reason, we have undertaken and provides the basis for later stages of feature a more extensive examination of vernier analysis. Barlow points to the very high density thresholds in cats. In the present study, we report measurements of vernier acuity made in visually intact cats using offsets in two sets of *Address correspondence to: S. Belleville, Dept. of Psycholhigh contrast square wave gratings of different ogy, 1205 Dr. Penfield Ave., Montreal, Quebec, Canada, spatial frequency. We also report vernier H3A IBI. INTRODUCTION
1’64
SYLVIE BELLEWLLEand FRASCES WILKINSON
thresholds measured using offsets in a set of single line stimuli.
locked. If an animal responded appropriately, it was reinforced with a preferred food (beef baby food); if however it jumped to the incorrect METHOD stimulus, the trap door opened and the cat fell a distance of 12 inches onto a soft surface. This Subjects reinforcement procedure was maintained during The subjects were five cats born and raised in both initial training and threshold measureour laboratory. Three of these were littermates ment. Our prior experience with the apparatus (MK78, MK79, and MK80). The cats were showed that if the animal was permitted to individually housed and were provided with delay in responding, its attention was distracted water and dry cat food ad iibitum. At the onset by other aspects of the apparatus. Conof threshold measurement, the cats ranged in sequently, the animals were allowed an initial age from 4 to 8 months (see Table 1). 30sec period to respond and were then gently prodded at regular intervals using a flat wooden Apparafus plunger which fits snuggly into the tunnel The animals were tested on a jumping stand behind the cat. The left-right position of the similar to that described by Mitchell et al. stimuli was varied randomly. After every trial, (1976). They were trained to jump from an the stimuli were systematically moved in order enclosed platform onto one of two stimuli which to keep constant any auditory cues. lay on Iockable trap doors. The height of the During the learning phase, the height of the jumping platform was adjustable. The walls of jumping platform was gradually increased from the jumping platform were flared so that the an initial level of 30cm to a final height of experimenter, positioned behind the animal, approximately 50 cm which then remained concould not see which stimulus the animal was stant throughout threshold evaluation (see looking at (latera head movem~ts~but could below). Thus, the viewing distance was always see if the animal was leaning below the floor of kept at or beyond the near points of accommothe platform. dation for cats as measured by Bloom and Berkley (1977). During the initial learning Stimuli period, we were very careful to prevent the Three stimulus sets were used: high contrast animal from attempting to lean toward the gratings of two spatial frequency (grating 1: stimuli before jumping. Cats that showed a 0.4 c/deg; grating 2: 1.1 c/deg) and single lines tendency to lean were discouraged by placing (21” long, 16’ wide). All stimuli were computer the experimenter’s hand just below the tunnel generated on a laser printer with a spatial exit. resolution of l/300 in. A series of offsets were We monitored viewing distance on a frequent produced, the sizes of which ranged from 49.5 basis throughout training and threshold delinto 1.1 minutes of visual angle (19 offset sizes per eation. In addition to the distance monitoring set). The grating stimuli subtended a total area done by the experimenters, some of the testing of 27” by 21”; grating 1 stimuli contained 13 sessions were videotaped. The position of the cyctes and grating 2 stimuli contained 29 cycles. animal’s eyes just prior to its jump was used as In the preceding description, visual angles are its viewing distance. We consider this as a based on a viewing distance of 50 cm since most conservative estimate as the animal may actuof our estimates were done from this distance ally make its choice from a greater distance (see below). The positive stimulus was a grating during its approach toward the edge of the or a single line with a horizontal offset at the jumping platform. The learning criterion was set to 90% correct midpoint of each line. The negative stimulus was an identical grating or single line without performance on 30 consecutive trials. Since the offset. The average luminance level measured at vernier task is highly learning dependent in the stimufi was 305 cd/m’. human adults (Westheimer and Hauske, 1975), the animals were given a large number of pracTraining procedure tice trials on various offset sizes after reaching As a first step, the animals were trained to criterion and before the measurement of their discriminate a grating with a large offset from a vernier thresholds. After completion of testing grating with no offset in 40 trial daily sessions. on any one of the three stimulus sets, the The door bearing the positive stimulus was animals were transferred to the next stimulus
Cat vernier acuity
(for which a criterion of 27130 correct responses was required), and were again given practice trials before their thresholds were measured. Threshold measurements
Two psychophysical procedures were employed to delineate the thresholds of our animals. Viewing distance remained constant throughout the threshold evaluation and was 50cm for all cats except for MK58 whose viewing distance was 47 cm. Modified staircase procedure. Within a 40-trial daily session the stimuli were presented in order of decreasing offset until the animal failed to respond correctly. A failure produced an increase of four steps in the offset series (66’ at 50 cm). This increase was followed by the presentation of the next stimulus in decreasing order of offset until the animal failed again. This was continued over the 40 trials. Animals were tested over a sufficient number of days to gather 50 to 130 trials at each near-threshold value. Method of constant stimuli. From the performance of the animal on the practice trials and from previous data from other anin&_lO offset values were chosen which were expected to bracket the threshold. These 10 offset values were presented in a random order. Four sets of 10 random presentations were given every day over a period of 20 days totalling 80 trials at each offset value. One cat (MK58) was tested using both psychophysical procedures but a single stimulus set (grating 1). The other four cats were tested on all three stimulus sets using a single psychophysical procedure (MK68: method of constant stimuli; MK78, MK79, and MK80: staircase procedure). All four were tested first with grating 1. Two cats, MK68 and MK78, were then tested according to the following sequence: grating 2, single line. The sequence was reversed for MK79 and MK80: single line, grating 2. Following this sequence, MK80’s threshold on grating 1 was retested at the original height
1265
(50 cm) and at a higher position
(75 cm). Assuming that we correctly estimated the position of the animal’s eyes in the first measure of the threshold, testing the animal from an increased distance should produce similar results. Table 1 indicates the psychophysical procedure used, as well as the order of testing on each stimulus for the five animals.
RESULTS
Table 1 shows the number of trials required to reach criterion for each of our subjects (range: 433-266 1). The variation observed in the number of trials required to learn the task may reflect individual differences or differences due to age at onset of testing. While the issue of age is an important one, and one which we are currently investigating, it will not be considered further in the present report because all our threshold measurements were made after 4 months of age and no age-related threshold differences were found (see below). Thresholds
The performance of each subject was plotted against offset size on a linear scale separately for each stimulus and/or measurement condition. Threshold was determined by fitting a straight line to each data set with regression analysis and by taking the offset value corresponding to the estimated 70% correct performance. We included in the regression analysis only the data points in the descending portion of the psychometric curve. In classifying data points as belonging to the descending portion we used the following criteria. Upper limit. Based on performance on the four largest offset values, we determined a confidence interval (2 SD) for asymptotic performance. The smallest offset value for which performance still fell within this range was taken as the top of the curve.
Table I. Training and testing histories for the five cats Cat
Age (days) at onset of training Trials to criterion Age (months) at threshold measurement Psychophysical procedure Stimulus order
MKSS
MK6S
MK7S
92 -925 s-10 SP_and a Gl
45 2661 7-9 cs GI-G2-SL
65 1042 4-6 SP GI-G2-SL
MK79 65 582 4-6 SP GI-SL-G2
MKSO 150 433 6-8 SP GI-SL-GZ-GI-GI’
‘This animal was retested on grating 1 from two different viewing distances (50 and 75 cm). CS: methodof constant stimuli; SP: staircase procedure; G I: grating 1 (0.4 c/deg); G2: grating 2 (1.1c/deg); SL: single line.
I266
SYLLIE BELLEVILLEand
When retested on grating 1, MK80 was found to have thresholds of 3.4’ and 3.6’ at the original viewing distance and at 75 cm respectivefy. These two values are very similar; they are also very close to MK80’s performance in the first testing on grating I (3.3’).
1X
DISCUSSION
The vernier task proved difficult for cats to learn, but when they had acquired it, they performed at a very high level with large offsets 2 4 6 a 10 12 14 16 and showed rapid falloff to chance performance Offset (min of arc) at small offset values, The offset thresholds measured in the five cats were found to range from 2.2’ to 6.7’. This range is not due to the use 100 of two different psychophysical procedures (staircase and constant stimuli) because the two 90 procedures when used in the same cat (MK58) . . 80 . yielded similar threshold values: 6.7 and 6.4’ for z . grating 1 (see Table 2). Since the role of practice ---__---___-__---y 70 8 u in achieving optimal vernier performance has . 8 60 Constant stimuli been emphasized in the human literature (WestMK58 . /-= heimer and Hauske, 1975) it is important to 50 note that all threshold values were determined -* 40 following extensive over-training on various ~, ,, , , , , , offset sizes. Furthermore, we did not find any 2 4 6 a 10 12 14 16 significant improvement as a function of Offset (mln of arc) presentation order, which might have been exFig. I. Frequency of seeing curves and fitted lines for MKS8 pected if the cats were not performing optimally tested on grating I using the staircase procedure (top) and on the earty tasks. Consequently, it is very the method of constant stimuli (bottom). probable that the thresholds we measured reflect the best performance of which our animals were Lotser hit. The smallest offset included was capable under the particular test conditions the largest offset for which performance did used. This conclusion receives further strong not differ significantly from chance (normal support from the data of MK80. This cat was approximation to the binomial distribution). The first cat, MK58, was tested using both the Table 2. Vernier acuity thresholds (70% cutoff criterion) for MK58 (a) and for MK68, MK78, MK79, MK80 (b). A staircase and the method of constant stimuli on second threshold estimate is given in brackets grating I. Figure 1 shows the frequency of MK58 seeing curves and the fitted lines for the two data sets. The estimated thresholds for this Staircase Constant stimuli (4 animal were 6.4 and 6.7’ on the staircase and Grating I constant stimuli respectively (Table 2a). The 70% threshold 6.4’ (4.2’) four remaining cats were tested on the three (60% cutoff) stimulus sets. Their frequency of seeing curves MK80 MK78 MK79 MK68 (b) and regression lines are shown in Fig. 2. The Grating -1 thresholds measured on all three stimuli ranged 3.3. 5.0 5.4 3.3‘ threshold from 2.2 to 6.1’ (Table 2b). As can be seen from 70% (2.7’) (4.1’) (2.6’) (4.2’) (60% cutoff) Table 2b, this overall range is quite representaGrating 2 tive of the range of values measured on each of 70% threshold 2.6’ 3.3’ 4.3’ 2.2’ (1.9’) (2.7’) the three stimulus patterns. The mean thresh- (60% cutoff) (1.6’) (3.6’) olds for each stimulus set are 4.7;iSDS 1.4) for Single line 4.6 3.1’ 6.1’ 3.3 grating 1, 3.I’(SD = 0.9) for grating 2, and 4.3’ 70% threshold (2.3’) (3.9’) (1.4’) (5.0’) (60% cutoff) (SD = 1.4) for the single line. 40
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Fig. 2. Frequency of seeing curves and fitted lines for four animals tested on grating I, grating 2. and on the single lines. A Indicates that the staircase procedure was used; 0 indicates that the method of constant stimuli was used.
retested on grating 1 at two different heights following completion of the grating l-grating 2-single line sequence, and showed thresholds almost identical to its initial threshold on grating 1 at both heights (3.4 and 3.6’ vs 3.39. The finding of identical thresholds at 50 and 75 cm is additional strong evidence that our viewing distance estimates were quite accurate.
One of the questions which motivated this study was whether thresholds in the hyperacuity range could be obtained on the vernier task if a more salient stimulus than the single line target of previous studies were employed. We thought the redundant nature of our grating stimuli might increase their salience. The issue of hyperacuity will be considered at length below; first,
1268
SYLLIE BELLEYILLEand FRASCES WILKISSOU
however, our findings must be compared directly with those of Berkley and Sprague (1979). Our cats did not show consistently better thresholds on the grating stimuli (grating 1 and grating 2) than on our single line stimulus, indicating that under our conditions, gratings and single lines are equally effective vernier targets. The thresholds reported by Berkley and Sprague (1979) and more recently by Berkley and Bush (1982) (4-8’) overlap the upper end of our range. It should be noted, however, that we have used a more conservative estimate of threshold (70% vs 56% correct). Since most of the behavioural studies of grating acuity to which we wish to compare our results (see below) use a 70% or 75% cutoff, this seemed the more appropriate choice. Berkley and Sprague’s cats maintained 70% performance at offset values of about 10’ of arc. Applying a less conservative cutoff criterion (60%) to our data yields threshold estimates that range from 1.4 to 5’ (see Table 2). Thus it would seem that our stimulus configuration supports somewhat better vernier offset detection. Although we found no difference between grating aiid Ogle line stimuli, it is possible that all our stimuli were more salient because they covered a much larger portion of the visual field than the 5’ segment line of the previous studies. In all cases, of course, the only relevant information is located within a very small region at the line centre. It should also be noted that the average luminance was at least I log unit higher in the present study. However, we doubt that luminance level is the critical factor because estimates of spatial acuity made under similar luminance conditions in our laboratory (Wilkinson and Belleville, unpublished observations) are not better than the ones reported by Berkley and Sprague (1979). We have recently learned that Mitchell and Murphy (personal communication) have obtained vernier thresholds of l-2’ of arc using the temporally displaced offset procedure introduced by Shimojo ef al. (1984) for human infants. Whether the detection of dynamic and static offsets reflects the same neural mechanism remains to be determined. Hyperacuity
The ability to detect vernier offsets has been termed a hyperacuity in humans because its threshold is considerably better than the spatial resolution of the system as determined by grating acuity or other spatial resolution measures.
Because of the efficient sampling strategy of the human visual system, spatial acuity approaches very closely the resolution limit imposed by diffraction in the human optical system (Krauskopf. 1962; Westheimer and Campbell, 1962). In the case of resolution acuity, the highly regular cone mosaic is fully exploited. Yet vernier exceeds this limit by an order of magnitude. Sampling at discrete points provides the information necessary to reconstruct the retinal image through interpolation (Barlow, 1981; Westheimer, 1979, 1981; Hirsch and Hylton, 1984: Snyder, 1982). Hirsch and Hylton (1984) have recently argued that the highly ordered hexagonal mosaic in the primate fovea provides the metric from which relative location in space can be determined even to accuracies in the hyperacuity range. It is widely assumed that the interpolation is caried out at the cortical level, and several authors (Barlow, 1979, 1981; Crick et al., 1980; Fahle and Poggio, 1983) have specifically pointed to layer IVC, a major target of the parvocellular geniculate laminae as a likely substrate. In primates, the cells in this layer have the same general receptive field structure as retinal ganglion and geniculate cells (Hubel and Wiesel, 1968, 1977; Blasdel and Fitzpatrick, 1984) but are much more numerous (O’Kusky and Colonnier, 1982). Hence they could serve to provide a very finegrained reconstruction of the information encoded by the retinal X-cells. Hyperacuity
in cats.?
In human subjects, behaviourally assessed spatial acuity coincides closely with the resoiution limit set by optical transmission and the cone mosaic, and hyperacuities are defined relative to this common limit. In cats, however, these three factors do not coincide so closely. Optical resolving power varies with pupil size (Robson and Enroth-Cugell, 1974; EnrothCugell and Robson, 1978; Woodhouse and Campbell, 1979) but under optimal conditions, values as high as 20 c/deg have been reported (Enroth-Cugell and Robson, 1978). Minimum intercone distance in region of peak cone density (area centralis) has been reported by Steinberg et al. (1973) to be 1.7’. If the cone mosaic set the limit for spatial resolution, one would predict a cutoff spatial frequency in the neighbourhood of 16 c/deg (exact value would depend on the nature of and degree of regularity in the mosaic). However, behavioural measures of cutoff spatial frequency for high contrast
Cat vernier acuity
gratings place the limit considerably below either the optical or the receptor limit (see below). It appears that the resolution of the cone mosaic is lost at the ganglion cell level, where even in the area centralis a considerable degree of convergence occurs (Stone, 1965; Steinberg er al., 1973; Hughes, 1975). Interpretation of ganglion cell densities is somewhat complicated by the fact that several classes of ganglion cell have been distinguished on the basis of their morphological and spatiotemporal response properties (reviewed by Stone, 1983), and at least two of these (alpha or Y cells and beta or X cells) can be further subdivided into off-centre and on-centre groups, The beta (X) cells show the highest spatial resolution (Cleland et al., 1979) and woutd hence be presumed to be important for detection of vernier offsets (Crick et al., 1981; Berkley and Bush, 1983; Zucker and Hummel, In press). On and off beta cells appear to form independent grids of approximately equal density. There is also some suggestion that the positions of cell pairs from the two grids are highly correlated (Wassle et al., i 98 1) suggesfig that the same spatial location is SimultaneousIy sampled by two channels. This has been interpreted by a number of investigators (Barlow, 1981; Fahle and Poggio, 198 1; Wassle et al., 1981) as indicating that the task of signalling intensity relative to local background is split into two parts (greater than and lower than background). On this basis, the spatial resolution of the visual system woutd be determined by the minimum interganglion cell distance in one of the two maps, a distance which Wassle et al. (1981) calculate as subtending a visual angle of 5.4’ of arc. The assumption that on and off grids operate independently has been questioned by Hughes (198 1). In the sort of heterogeneous model he proposes, thresholds up to 10 c/deg co&d be supported. Thus anatomical considerations do not provide a clear estimate of the resolution of the information leaving the retina. The spatial resolution of the cat’s visual system has been assessed both behaviourally (Smith, 1936; Blake et al., 1974; Muir and ~itchell,l975; Jacobson et al., 1976; Mitchell et al., 1977; Pasternak and Merigan, 198-l; Elberger, 1982) and by evoked potentials (Berkley and Watkins, 1973; Campbell et gl., 1973; Harris, 1978) and values ranging from below 3 c/deg to over lOc/deg have been reported. The interactive role of several factors
1269
(luminance, total stimulus area, motivational conditions, threshold definition) in determining this range is not yet fully understood. Abasing (‘Williams and Collier, 1983; Yellott, 1983) must also be considered a possible contributing factor to the highest values reported. If we use one of the highest reported behavioural cutoffs (9c/deg) (Jacobson et al., 1976), an average cutoff (6 c/deg) (Blake et al., 1974), and one of the lowest under photopic conditions (3 c/deg) (Pasternak and Merigan, 1981) as examples, the best vernier acuity for which no special interpolation would be required woutd be 3.3, 5 and 10’ respectively. We have not tested spatial acuity in the cats used in this study; however, other cats tested in our laboratory under similar test procedures (including threshold criterion and lighting conditions) to those used for the vernier task routinely produce acuity cutoffs in the 4-4.5 c/deg range which applied to vernier threshold predicts a limit of about 7’ without interpolation. Thus based on spatial acuity measurements, one must conclude that if the cat’s vernier acuity is in the hyperacuity range the interpolated representation provides an improvement in grain of not greater than three times, much less than the order of magnitude differences seen in the human. It should be noted that stereoacuity thresholds in the cat show a spatial precision similar to that reported here for vernier detection (4-10 min of arc disparity) (Kaye et al., 1981; Timney, 1981, 1983, 1984). This observation is interesting because it indicates that two abilities which are in the hyperacuity range in humans are spatially limited to a similar extent in the cat. This is suggestive of a common neural substrate at an early stage of visual processing (Berry, 1948; Stigmar, 1970). That substrate is likeiy to involve the X-cellinput target cells in striate cortex (Berkley and Bush, 1984; Crick et at., 1981). As discussed above, the large numerical difference between geniculate input fibres and cortical cells in layer IVC/3 of primates has led to speculation about their involvement in the interpolation process. In the cat, the ratio of geniculate projection cells to area 17 target ceiis is certainly smalier than in the primate: Beaulieu and Colonnier (1983) estimate l/20 in cats (Layer IV) and l/55 in monkeys (Layer IVA and IVC). Another difference between cat and primate which may prove significant in this context is that the receptive field properties of the layer IV target cells which receive X-cell input are dissimilar.
SL LL IE BELLE~ILLE and FR;\.UCES WILI;IXOZ
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As documented initially by Hubel and Wiesel (1968. 1977). and confirmed bv others (BIasdell and Fitzpatrick, 1984). the cells of layer IVC in the primate are monocularly activated and have nonoriented receptiv-e fields. In the cat. on the other hand. cells in layer IV which receive direct X-cell input are predominantly simple cells with elongated receptive fields (Bullier and Henry, 1979; Gilbert and Wiesel, 1979). The proportion of nonoriented cells in layer IV in the cat is much smaller than in the primate (Bullier and Henry, 1979, 1980). Perhaps these differences account for the modest degree of spatial interpolation which our data indicate in the cat. ,~cli,ton/erfgemeItts-We would like to thank Yvan Leclerc and Dr Steven Zucker for their help in producing the stimuli. This study was supported by NSERC grant No. 7551 to F.W.
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