- Email: [email protected]
Contrast discrimination in the cat
Behavioural Brain Research, 12 (1984) 155-162
155
Elsevier BBR 00351
CONTRAST DISCRIMINATION IN THE CAT
R A N D O L P H BLAKE and I S M E N E PETRAKIS
Departments of Psychology and Neurobiology/Physiology, Cresap Neuroscience Laboratory, Northwestern University, Evanston, IL 60201 (U.S.A.) (Received January 4th, 1984) (Revised version received February 28th, 1984) (Accepted March 3rd, 1984)
Key words: contrast discrimination - vision - grating pattern - cat
Cats were trained to discriminate between two sinusoidal grating patterns differing only in contrast. The smallest discriminable contrast difference was determined for a number of different baseline contrast levels, and the resulting contrast increment thresholds plotted in the form of a contrast discrimination function. The resulting function was linear when plotted on log/log coordinates and the slope of this function varied with spatial frequency. These behavioural results are compared to the contrast/response properties of retinal and cortical neurones.
INTRODUCTION
Behavioural studies show that the cat's ability to detect a grating pattern depends strongly on the spatial frequency of that pattern 3,4. In effect, the visual system of the cat behaves like a band-pass filter, delimiting the range of visible spatial frequencies to 5 or 6 octaves. Moreover, it appears that within this range the cat uses more narrowly tuned mechanisms when detecting a particular spatial frequency,judging from the effects of visual masking noise on detection performance 5. The results from these threshold studies indicate that the cat's ability to detect grating patterns can be related, at least qualitatively, to the response properties of neurones within the cat's visual system (e.g. see ref. 18). Encouraged by this correspondence between psychophysics and physiology, we have extended this behavioral analysis of cat spatial vision to suprathreshold contrast levels. There are several reasons for wanting to examine the cat's visual performance at contrast levels well above threshold. First, from physiological studies a great deal is known about the 0166-4328/84/$03.00 © 1984 Elsevier Science Publishers B.V.
effect of grating contrast on the response amplitude of neurones in the cat's retina 19 and brain 9. Behavioral studies enable us to examine the extent to which suprathreshold contrast perception can be understood in terms of the contrast/response properties of these neurones. Second, there are several studies describing suprathreshold contrast perception in humans 11"16, and efforts to model those data are sometimes based on neurophysiological results from the cat 7. In order to justify generalizing from cat neurophysiology to human psychophysics, it is important to assess the performance of cat and human on comparable tasks. To study suprathreshold contrast perception in the cat, we determined the cat's ability to discriminate sinusoidal grating patterns differing in contrast only. This kind of task has been widely employed in the study of human contrast perception l°-12A6"21. In the present experiment, the cat viewed a pair of grating patterns, one of contrast C and the other of contrast C + AC; the cat was trained to select the pattern of higher contrast. Fig. 1 illustrates the kind of test display viewed by the cat; the contrast of the grating on the left is
156
Fig. I. This pair of vertical, sinusoidal grating patterns illustrates the stimulus display seen by the cat on each trial. The cat was trained to select the grating of higher contrast, which in this case is the pattern on the left. This pair of gratings differs in contrast by 0.3 log-units. 0.30 log-units higher than the contrast of the grating on the right. Within a block of trials, the value of C (the background contrast) remained constant while AC (the increment) was varied. For each background contrast value, we found the smallest contrast difference that could be reliably discriminated by the cat, a value termed the contrast increment threshoM. This procedure was repeated for a number of background contrast values, and the resulting set of increment thresholds plotted as a contrast discrimination function. This function provides a quantitative description of suprathreshold contrast processing that can then be compared to the contrast gain functions for individual neurones. METHODS Procedures and apparatus A two-alternative, spatial forced-choice procedure was used to measure contrast increment thresholds. During daily testing sessions, the cat was comfortably housed in a restraining box. Located on one wall of the box was a circular window through which the cat could extend its head, as shown in Fig. 2. Located directly in front of this window were two matched cathode ray tube (CRT) displays. Each CRT was masked to a circular area 16 ° visual angle in diameter; the nearest edges of the two CRT displays were separated by 8 o. This relatively large display size insured that even at the lowest spatial frequency tested, the grating contained many cycles of the
waveform. The CRT displays and restraining box were housed within a darkened chamber, with the only source of illumination provided by the CRT displays. Auditory white noise was broadcast into the test chamber to mask extraneous sounds. An infrared-sensitive camera mounted above the CRT displays allowed the experimenter to observe the cat over a closed-circuit television. Conventional electronic techniques were used to generate rasters on both CRTs; the mean luminance was 27 cd/m 2, a value enabling us to achieve contrast levels up to 0.50 without exceeding the linear intensity range of the CRTs. With natural pupils, this light level falls in the low photopic range for the cat. Vertical sine-wave gratings could be presented on either or both CRTs by applying a sinusoidal signal to the Z-axis amplifier(s). Using a programmable attenuator under computer control, grating contrast could be varied independently on the two CRTs in 1 dB (0.05 log-unit) steps. (We employ the conventional definition of contrast, the difference between the maximum and minimum intensities of the waveform divided by their sum.) To avoid abrupt transients, gratings were always introduced and withdrawn gradually over a 250 ms period using a shaped rise/fall gate. The cat viewed this pair of displays from a distance of 30 cm, a value within the animal's accommodative range 6. This rather close viewing distance was chosen in order to maximize the angular subtense of the displays. Located between the cat and the displays was a device for registering responses and delivering food reinforcements. Two nose-keys, one aligned with each CRT, were placed just below eye level and within easy reach of the cat. Situated midway between these nose-keys was a small metal tube through which a small amount of pureed beef could be delivered. Using standard operant procedures 2, the cat was trained to touch with its nose the key aligned with the CRT upon which a grating was displayed. During initial training, the other CRT remained evenly illuminated. Correct responses were rewarded by the delivery of food. The 'correct' CRT was varied randomly from trial to trial, with the stipulation that the test grating appear on the same side no more than 6 consecu-
157
Fig. 2. Ilustration of apparatus. While housed in a roomy restraining box (partially shown in cutaway), the cat extended its head through a porthole in order to view a pair of CRT displays. The cat selected with CRT, lett or fight, displayed the grating of higher contrast by touching its nose against one of two response keys situated between the cat and the displays. Correct choices were rewarded by delivery of food through the tube extending toward the cat. Shown just above the CRT displays is the closed circuit television camera, and above the camera is a small speaker through which auditory noise was broadcast to mask extraneous sounds. tive trials. A correction procedure was instituted whenever the cat r e s p o n d e d to the same nose-key more than 6 times in a row. Positional biases o f this sort were c o m m o n during initial training but seldom occurred once the task was mastered. Once trained on this simple detection task, the cat graduated to a contrast discrimination task. N o w on each trial gratings were presented on both C R T s , and the animal was reinforced with food for choosing the C R T displaying the grating
o f higher contrast. The spatial frequency and phase (relative to the edges o f the circular mask) o f the left-hand and right-hand gratings were identical, so that the cat had to base its judgement on contrast differences between the two gratings. E a c h trial consisted o f the following sequence o f events. A clearly audible tone informed the cat that a trial was underway, meaning that both C R T s displayed gratings. If the cat failed to r e s p o n d at all within 10 s, the animal was
158 penalized with a 5 s timeout period during which the gratings were removed and food was unavailable. If the cat responded correctly within the 10 s test period, the gratings were removed and the cat was rewarded with the delivery of a small quantity of food; the next trial followed 3 s after delivery of the food. If the cat responded incorrectly, the gratings were removed, food was withheld, and the animal had to wait 5 s before the next trial. The cat was discouraged from responding between trials by postponing the next trial 1 s each time the cat contacted either nose-key when the tone was not on; this contingency was easily learned, as evidenced by the cat's reluctance to touch the nose-keys except during test trials. Formal testing was initiated only after the cat consistently exceeded 90~o correct performance for 5 days in a row on a simple version of this contrast discrimination task (gratings differing in contrast by 0.3 log-units). When this level of performance was achieved, a staircase procedure 22 was implemented to determine the minimum contrast increment which could be discriminated at the 70 ~o correct level of performance. Two correct .choices in a row at one contrast level produced a reduction in the increment contrast; one incorrect choice produced an increase in the increment contrast. Initially the staircase moved in 6 dB steps; following the first reversal in the direction of the staircase the step size became 3 dB; and after the second reversal, the step size was reduced to 1 dB and remained at this value for the rest of the staircase. The staircase was terminated once a total of 15reversals had occurred. Contrast increment threshold was defined as the average contrast increment associated with the last 6 reversals. Each staircase typically consisted of 50-60 trials, and each daily testing session consisted of 4 consecutive staircases all devoted to the same test condition. Further details of the test conditions are given in the Results section. Cats Two normal, adult female cats participated in these experiments. Neither had prior experience on this two-choice discrimination task, so extensive training was administered prior to formal
data collection. During training and testing, the cats were maintained on a 23-h food deprivation schedule whereby they received their entire daily ration of food during the testing session. The food reward was a specially prepared diet consisting of pureed beef, powdered cat chow and vitamins. Both cats maintained at least 95 ~o normal body weight throughout the experiment, and both were regularly examined for any signs of malnutrition, dehydration or other health irregularities. RESULTS
Experiment 1 In the first experiment, contrast increment thresholds were measured for two different spatial frequencies, 0.5 cycles/degree and 1.5 cycles/degree. In view of the spatial tuning of visual neurones (e.g. see ref. 15), we assumed that these two spatial frequencies would probably activate different populations of visual neurones. Results from one of the cats tested in this first experiment appear in Fig. 3, which plots on log/log coordinates contrast increment thresholds as the function of background contrast. Each data point is the arithmetic mean of at least 8 threshold estimates. Open symbols show the results for the lower spatial frequency and filled symbols the results for the higher spatial frequency; the pair of error bars appearing on each set of data specify + 1 standard error, and the two members of each pair show the largest and smallest standard error for that condition. Across both conditions, standard errors averaged 9~o (i.e. less than 1 dB) of the mean. The two arrows along the ordinate denote the contrast thresholds for detection of these spatial frequencies in the absence of any background contrast. As already known, the cat is more sensitive (i,e. contrast threshold is lower) at 0.5 cycles/degree than at 1.5 c y c l e s / d ~ e e , which is why these two threshold values fall at different points along the ordinate. A least squares criterion was employed to fit a straight line to each set of increment thresholds. The slopes of these resulting lines are given in the figure inset. Clearly, the contrast discrimination function is steeper for the lower spatial frequency than it is for the higher one. This same pattern of
159
Stationary •
ll
.10
oo
J
-¢ .o~
J
o 0.5 c/d (.70) 0
•
1,5 c/d
(.-54)
Oe-
!
.~t DI
I
(~
. 3
I
I
I I I II
,10
I
I
.30
Background contrast
Fig. 3. Contrast discrimination functions for one cat at two spatial frequencies, 0.5 cycles/degree (open symbols) and 1.5 cycles/degree (filled symbols). Data points are the arithmetic mean of at least 8 threshold estimates, each obtained using a forced-choice staircase procedure. The error bars show + 1 S.E.M., and the pair of error bars shown for each function represent the largest and the smallest standard error for that condition. The arrows show contrast thresholds in the absence of a background grating. The slopes of the best fitting straight lines are given in parentheses within the inset. The correlation coefficient for the best fitting straight lines are 0.94 and 0.88 for the low and the high spatial frequency, respectively.
results was also found for the other cat (slope = 0.86 at 0.5 cycles/degree, with a correlation coefficient of 0.94; slope = 0.53 at 1.5 cycles/degree, with a correlation coefficient of 0.87).
Experiment 2 In the first experiment, a steady contrast increment was added to a steady background contrast to produce the grating of higher contrast. The contrast increment, in other words, contained no temporal modulation relative to the background. (Of course, the retinal image of the combined background and increment will undergo some degree of temporal modulation, owing to eye movements). One could argue, therefore, that this condition selectively activates neural mechanisms responsive to sustained contrast levels. We wondered whether contrast discrimination performance would change when the contrast increment consisted of a temporal modulation in contrast presented against a steady background level.
To answer this question, the following experiment was performed. In this second experiment, the contrast increment consisted of a sinusoidal modulation in contrast, whereby the increment was steadily introduced and removed at a fixed temporal frequency. Such a test stimulus can be considered as the sum of a steady grating (the background component) and an 'ON/OFF' flickering grating (the contrast increment). So, on each trial one CRT displayed the background component only while the other CRT displayed the background plus the temporally modulated contrast increment. The cat was reinforced for selecting the modulated contrast increment. As in the previous experiment, we measured contrast increment thresholds for different levels of background contrast. This was done for two rates of temporal modulation, 1.5 Hz and 8 Hz, at both 0.5 cycles/degree and 1.5 cycles/degree. Results from one Cat are summarized in Fig. 4. The left panel shows increment thresholds for the 1.5 Hz condition and the right panel the results for the 8 Hz condition; standard errors were comparable to those plotted in Fig. 3. Again, the bestfit lines reveal that contrast increment functions are steeper for the lower spatial frequency (slope values are given in parentheses within the figure). Also, for a given spatial frequency the function is steeper for the lower temporal frequency. This tendency is most pronounced at 1.5 cycles/degree, where thresholds for the 8 Hz contrast increment vary hardly at all with the background contrast. Complete functions were not obtained from the other cat, but selected points revealed the same trends as those seen in Fig. 4. DISCUSSION
The present results clearly show that the cat's ability to discriminate contrast increments depends upon the background contrast against which that increment is presented. In particular, increment thresholds increase with background contrast. Within the range of background contrast values studied, this relationship is adequately described by a straight line plotted on log/log coordinates. Contrast increment thresholds do
160
.50
I
1.5 hz
"
8 hz
.50
u'J 0 to ¢.)
.10
(.7o) o 0.5 c/d (.521 • 1.5 c/d
e,....~o~
4--
¢:
E
0
(.60) (.14)
o.lO /
.10
~ o /
0
t,.
co ¢-
-- .05
.05 I .05
I .10
I .50
Background
I
I
I
.03
.10
,50
contrast
Fig. 4. Contrast discrimination functions for one cat at two temporal frequencies, 1.5 and 8 Hz. The details are as in Fig, 3.
not increase as a constant proportion of the background (i.e. the slope of the contrast increment function is less than 1.0), thus indicating a departure from Weber's law. This departure is noteworthy, since evidence for Weber's law has been obtained in the cat on an increment detestion task where the display consisted of a large, circular spot of white light seen against a uniform background 13. This display could be construed as a low spatial frequency target appearing against an even lower (approaching zero) spatial frequency background. Considered together, these previous findings and the present results imply that the slope of the contrast increment function becomes steeper at lower spatial frequencies. The slope of the contrast discrimination function (as indexed by the slope of the best-fitting line in log/log coordinates) varies with spatial frequency, being steeper for the lower spatial frequency. Testing with temporally modulated contrast increments served further to exaggerate these differences between low and high spatial frequency gratings. This same pattern of results was found by Burbeck and Kelly7 in their study of contrast discrimination in humans. In their experiment, test and background patterns differed in orientation, but otherwise their procedures resembled those used in the present study. In other studies involving human observers, contrast
increment thresholds have been measured using briefly flashed grating p a t t e l ' n s !°,ll,16AT. Under those conditions, spatial frequency has minimal effect on the slopes of the resulting contrast discrimination functions - the resul~g slope values fall in the neighbourhood of 0:7, a value close to that found for the cat at 0.5 cycles/degree.
Physiological implications Are there response properties of cat visual neurones that might account for these behavioural findings? To address this question, several assumptions must be made concerning the nature of this contrast discrimination task. First, we assume that increases in background contrast produce a monotonic increase in the response amplitude of visual neurones. Ignoring saturation effects, this assumption is supported by physiological data 1,9"14, Second, we assume that increment threshold performance depends on a fixed, criterion difference between the response to the background alone and the response to the background plus increment. This is a fairly standard assumption in threshold studies. Now given these assumptions, let us consider possible physiological correlates of two aspects of the present findings, beginning with the departure from Weber's law. Physiological measurements have established that many cortical cells exhibit a compressive
161 non-linearity (e.g. see ref. 1). In other words, the slope of the function relating response to contrast becomes shallower at intermediate and high contrast levels. This means that to elicit a just discriminable increase in neural activity, larger increments in contrast are required at higher contrast levels. This neural response compression could underly the compressive nature of the contrast discrimination function. In fact, Albrecht and Hamilton I fotmd that in their large sample of cat cortical cells, the average slope of the contrast response function was 0.59; for purposes of comparison, the average of all the slope values for the contrast discrimination functions shown in Figs. 3 and 4 equals 0.54. Considering next the variation in the slope of the contrast discrimination function with spatial frequency, we have considered two possible explanations for this finding. First, it could be that a single neural mechanism underlies discrimination performance at all spatial frequencies and that the gain of this single mechanism (i.e. the growth of response with contrast) changes with spatial frequency. In fact, there is physiological evidence that individual cortical cells exhibit just such behavior, with each cell showing its greatest gain at the optimal spatial frequency for that cell9. However, this explanation does not fit well with other psychophysical evidence indicating that the cat utilizes different neural mechanisms when detecting spatial frequencies differing by an octave or more 5. Based on those findings, we would expect the cat to utilize that mechanism exhibiting the greatest contrast gain for the condition under test, a strategy yielding the largest number of correct choices. According to this second hypothesis; the cat, when tested at 0.5 cycles/degree, would utilize a different population of neurones than those utilized when tested at 1.5 cycles/degree. Is there physiological evidence for variations in contrast gain among different classes of visual neurones? Considering first cat retinal ganglion ceils, it has been reported that Y cells exhibit steeper contrast/response functions than do X cells 19. There is also evidence that Y cells are more responsive than X cells at lower spatial frequencies, while at higher spatial frequencies this tendency is re-
versed 8. (Incidentally, these physiological measurements were performed at light levels comparable to that used in our behavioural work.) So considered together, these physiological properties of X and Y cells imply that contrast discrimination should be better at low spatial frequencies (where the contrast/response function is steeper), which it is. However, this suggestive parallel between psychophysics and physiology disappears when we examine the response properties of striate cortex neurones. Among striate units, the steepest contrast/response functions are exhibited by those cells classified as 'special complex', but there is no tendency for this class of cortical cells to respond to lower spatial frequencies9. And there are certainly no clear differences between the contrast/response functions of simple cells and regular complex cells 2'9, the two cell types thought by some to be the cortical analogues of the retinal X and Y cells 2°. So at present, the evidence linking contrast discrimination to particular classes of visual neurones remains rather weak. Finally, Fig. 4 indicates that at 1.5 cycles/degree (a high spatial frequency for the cat) a stationary background grating has virtually no effect on the cat's ability to detect a contrast increment temporally modulated at 8 Hz. Evidently the neural mechanism mediating detection of the transient modulation in contrast is unaffected by the steady background. One might attempt to explain this lack of interaction between a transient stimulus and a steady one in terms of sustained and transient visual neurons, a dichotomy that has been popularized in recent theorizing. However, the absence of similar trends at the lower spatial frequency (0.5 cycles/degree) makes us cautious in advancing such an interpretation. ACKNOWLEDGEMENTS
This work was supported by grants from the National Institutes of Health (EY01596) and from the Alumnae Board of Northwestern University. We are grateful to Karen Holopigian, Karin Boothroyd, Gregory Phillips and Geoffrey Iverson for helpful discussion. I.P. is now at the University of Pittsburgh Medical School.
162 REFERENCES 1 Albrecht, D.G. and Hamilton, D.B., Striate cortex of monkey and cat: contrast response function, J. Neurophysiol., 48 (1982) 217-237. 2 Berkley, M.A., Visual discriminations in the cat. In W.C. Stebbins (Ed.), Animal Psychophysics: The Design and Conduct of Sensory Experiments, Appleton-CenturyCrofts, New York, 1970, pp. 231-247. 3 Bisti, S. and Maffei, L., Behavioural contrast sensitivity of the cat in various visual meridians, J. Physiol. (Lond.), 241 (1974) 201-210. 4 Blake, R., Cool, S.J. and Crawford, M.L.J., Visual resolution in the cat, Vision Res., 14 (1974) 1211-1217. 5 Blake, R. and Martens, W., Critical bands in cat spatial vision, J. Physiol. (Lond.), 314 (1981) 175-187. 6 Bloom, M. and Berkley, M.A., Visual acuity and the near point of accommodation in cats, Vision Res., 17 (1977) 723-730. 7 Burbeck, C.A. and Kelly, D.H., Contrast gain measurements and the transient/sustained dichotomy, J. Opt. Soc. Amer., 71 (1981) 1335-1342. 8 Cleland, B.G., Harding, T.H. and Tulanay-Keesey, U., Visual resolution and receptive field size: examination of two kinds of cat retinal ganglion cell, Science, 205 (1979) 1015-1017. 9 Dean, A.F., The relationship between response amplitude and contrast for cat striate cortical neurones, J. Physiol. (Lond.), 318 (t981) 413-427. 10 Legge, G.E., Spatial frequency masking in human vision: binocular interactions, J. Opt. Soc. Amer., 69 (1979) 838-847. 11 Legge, G.E., A power law for contrast discrimination, Vision Res., 21 (1981) 457-467.
12 Legge, G.E. and Foley, J.M., Contrast masking in human vision, J. Opt. Soc. Amer., 70 (1980) 1458-1471. 13 Loop, M.S. and Millican, C.L., Increment thresholds in normal and binocularly deprived cats, Behav. Brain Res.. 9 (1983) 143-150. 14 Maffei, L. and Fiorentini, A., The visual cortex as a spatial frequency analyser, Vision Res., 13 (1973) 1255-1267. 15 Movshon, J.A., Thompson, I.D. and Tolhurst, D.J., Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex, J. Physiol. (Lond.), 283 (1978) 101-120. 16 Nachmias, J. and Sansbury, R., Grating contrast discrimination may be better than detection, Vision Res., 14 (1974) 1039-1042. 17 Pantle, A., Simultaneous masking of one spatial sine wave by another, Invest. Ophthal. vis. Sci., Suppl. 16 (1977) 47. 18 Robson, J.G., Receptive fields: spatial and intensive representation of the visual image. In D. Carterette and W. Friedman (Eds.), Handbook of Perception, Vol. 5, Academic Press, New York, 1975, pp. 81-112. 19 Shapley, R.M. and Victor, J.D., The effect of contrast on the transfer properties of cat retinal ganglion cells, J. Physiol. (Lond.), 285 (1978) 275-298. 20 Stone, J. and Dreher, B., Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex, J. Neurophysiol., 36 (1973) 551-567. 21 Swanson, W.H., Wilson, H.R. and Giese, &C., Contrast matching data predicted from contrast increment thresholds, Vision Res., 24 (1984) 63-75. 22 Wetherill, G.B. and Levitt, H., Sequential estimation of points on a psychometric function, Brit. J. math, stat. Psychol., 18 (1965) 1-10.
155
Elsevier BBR 00351
CONTRAST DISCRIMINATION IN THE CAT
R A N D O L P H BLAKE and I S M E N E PETRAKIS
Departments of Psychology and Neurobiology/Physiology, Cresap Neuroscience Laboratory, Northwestern University, Evanston, IL 60201 (U.S.A.) (Received January 4th, 1984) (Revised version received February 28th, 1984) (Accepted March 3rd, 1984)
Key words: contrast discrimination - vision - grating pattern - cat
Cats were trained to discriminate between two sinusoidal grating patterns differing only in contrast. The smallest discriminable contrast difference was determined for a number of different baseline contrast levels, and the resulting contrast increment thresholds plotted in the form of a contrast discrimination function. The resulting function was linear when plotted on log/log coordinates and the slope of this function varied with spatial frequency. These behavioural results are compared to the contrast/response properties of retinal and cortical neurones.
INTRODUCTION
Behavioural studies show that the cat's ability to detect a grating pattern depends strongly on the spatial frequency of that pattern 3,4. In effect, the visual system of the cat behaves like a band-pass filter, delimiting the range of visible spatial frequencies to 5 or 6 octaves. Moreover, it appears that within this range the cat uses more narrowly tuned mechanisms when detecting a particular spatial frequency,judging from the effects of visual masking noise on detection performance 5. The results from these threshold studies indicate that the cat's ability to detect grating patterns can be related, at least qualitatively, to the response properties of neurones within the cat's visual system (e.g. see ref. 18). Encouraged by this correspondence between psychophysics and physiology, we have extended this behavioral analysis of cat spatial vision to suprathreshold contrast levels. There are several reasons for wanting to examine the cat's visual performance at contrast levels well above threshold. First, from physiological studies a great deal is known about the 0166-4328/84/$03.00 © 1984 Elsevier Science Publishers B.V.
effect of grating contrast on the response amplitude of neurones in the cat's retina 19 and brain 9. Behavioral studies enable us to examine the extent to which suprathreshold contrast perception can be understood in terms of the contrast/response properties of these neurones. Second, there are several studies describing suprathreshold contrast perception in humans 11"16, and efforts to model those data are sometimes based on neurophysiological results from the cat 7. In order to justify generalizing from cat neurophysiology to human psychophysics, it is important to assess the performance of cat and human on comparable tasks. To study suprathreshold contrast perception in the cat, we determined the cat's ability to discriminate sinusoidal grating patterns differing in contrast only. This kind of task has been widely employed in the study of human contrast perception l°-12A6"21. In the present experiment, the cat viewed a pair of grating patterns, one of contrast C and the other of contrast C + AC; the cat was trained to select the pattern of higher contrast. Fig. 1 illustrates the kind of test display viewed by the cat; the contrast of the grating on the left is
156
Fig. I. This pair of vertical, sinusoidal grating patterns illustrates the stimulus display seen by the cat on each trial. The cat was trained to select the grating of higher contrast, which in this case is the pattern on the left. This pair of gratings differs in contrast by 0.3 log-units. 0.30 log-units higher than the contrast of the grating on the right. Within a block of trials, the value of C (the background contrast) remained constant while AC (the increment) was varied. For each background contrast value, we found the smallest contrast difference that could be reliably discriminated by the cat, a value termed the contrast increment threshoM. This procedure was repeated for a number of background contrast values, and the resulting set of increment thresholds plotted as a contrast discrimination function. This function provides a quantitative description of suprathreshold contrast processing that can then be compared to the contrast gain functions for individual neurones. METHODS Procedures and apparatus A two-alternative, spatial forced-choice procedure was used to measure contrast increment thresholds. During daily testing sessions, the cat was comfortably housed in a restraining box. Located on one wall of the box was a circular window through which the cat could extend its head, as shown in Fig. 2. Located directly in front of this window were two matched cathode ray tube (CRT) displays. Each CRT was masked to a circular area 16 ° visual angle in diameter; the nearest edges of the two CRT displays were separated by 8 o. This relatively large display size insured that even at the lowest spatial frequency tested, the grating contained many cycles of the
waveform. The CRT displays and restraining box were housed within a darkened chamber, with the only source of illumination provided by the CRT displays. Auditory white noise was broadcast into the test chamber to mask extraneous sounds. An infrared-sensitive camera mounted above the CRT displays allowed the experimenter to observe the cat over a closed-circuit television. Conventional electronic techniques were used to generate rasters on both CRTs; the mean luminance was 27 cd/m 2, a value enabling us to achieve contrast levels up to 0.50 without exceeding the linear intensity range of the CRTs. With natural pupils, this light level falls in the low photopic range for the cat. Vertical sine-wave gratings could be presented on either or both CRTs by applying a sinusoidal signal to the Z-axis amplifier(s). Using a programmable attenuator under computer control, grating contrast could be varied independently on the two CRTs in 1 dB (0.05 log-unit) steps. (We employ the conventional definition of contrast, the difference between the maximum and minimum intensities of the waveform divided by their sum.) To avoid abrupt transients, gratings were always introduced and withdrawn gradually over a 250 ms period using a shaped rise/fall gate. The cat viewed this pair of displays from a distance of 30 cm, a value within the animal's accommodative range 6. This rather close viewing distance was chosen in order to maximize the angular subtense of the displays. Located between the cat and the displays was a device for registering responses and delivering food reinforcements. Two nose-keys, one aligned with each CRT, were placed just below eye level and within easy reach of the cat. Situated midway between these nose-keys was a small metal tube through which a small amount of pureed beef could be delivered. Using standard operant procedures 2, the cat was trained to touch with its nose the key aligned with the CRT upon which a grating was displayed. During initial training, the other CRT remained evenly illuminated. Correct responses were rewarded by the delivery of food. The 'correct' CRT was varied randomly from trial to trial, with the stipulation that the test grating appear on the same side no more than 6 consecu-
157
Fig. 2. Ilustration of apparatus. While housed in a roomy restraining box (partially shown in cutaway), the cat extended its head through a porthole in order to view a pair of CRT displays. The cat selected with CRT, lett or fight, displayed the grating of higher contrast by touching its nose against one of two response keys situated between the cat and the displays. Correct choices were rewarded by delivery of food through the tube extending toward the cat. Shown just above the CRT displays is the closed circuit television camera, and above the camera is a small speaker through which auditory noise was broadcast to mask extraneous sounds. tive trials. A correction procedure was instituted whenever the cat r e s p o n d e d to the same nose-key more than 6 times in a row. Positional biases o f this sort were c o m m o n during initial training but seldom occurred once the task was mastered. Once trained on this simple detection task, the cat graduated to a contrast discrimination task. N o w on each trial gratings were presented on both C R T s , and the animal was reinforced with food for choosing the C R T displaying the grating
o f higher contrast. The spatial frequency and phase (relative to the edges o f the circular mask) o f the left-hand and right-hand gratings were identical, so that the cat had to base its judgement on contrast differences between the two gratings. E a c h trial consisted o f the following sequence o f events. A clearly audible tone informed the cat that a trial was underway, meaning that both C R T s displayed gratings. If the cat failed to r e s p o n d at all within 10 s, the animal was
158 penalized with a 5 s timeout period during which the gratings were removed and food was unavailable. If the cat responded correctly within the 10 s test period, the gratings were removed and the cat was rewarded with the delivery of a small quantity of food; the next trial followed 3 s after delivery of the food. If the cat responded incorrectly, the gratings were removed, food was withheld, and the animal had to wait 5 s before the next trial. The cat was discouraged from responding between trials by postponing the next trial 1 s each time the cat contacted either nose-key when the tone was not on; this contingency was easily learned, as evidenced by the cat's reluctance to touch the nose-keys except during test trials. Formal testing was initiated only after the cat consistently exceeded 90~o correct performance for 5 days in a row on a simple version of this contrast discrimination task (gratings differing in contrast by 0.3 log-units). When this level of performance was achieved, a staircase procedure 22 was implemented to determine the minimum contrast increment which could be discriminated at the 70 ~o correct level of performance. Two correct .choices in a row at one contrast level produced a reduction in the increment contrast; one incorrect choice produced an increase in the increment contrast. Initially the staircase moved in 6 dB steps; following the first reversal in the direction of the staircase the step size became 3 dB; and after the second reversal, the step size was reduced to 1 dB and remained at this value for the rest of the staircase. The staircase was terminated once a total of 15reversals had occurred. Contrast increment threshold was defined as the average contrast increment associated with the last 6 reversals. Each staircase typically consisted of 50-60 trials, and each daily testing session consisted of 4 consecutive staircases all devoted to the same test condition. Further details of the test conditions are given in the Results section. Cats Two normal, adult female cats participated in these experiments. Neither had prior experience on this two-choice discrimination task, so extensive training was administered prior to formal
data collection. During training and testing, the cats were maintained on a 23-h food deprivation schedule whereby they received their entire daily ration of food during the testing session. The food reward was a specially prepared diet consisting of pureed beef, powdered cat chow and vitamins. Both cats maintained at least 95 ~o normal body weight throughout the experiment, and both were regularly examined for any signs of malnutrition, dehydration or other health irregularities. RESULTS
Experiment 1 In the first experiment, contrast increment thresholds were measured for two different spatial frequencies, 0.5 cycles/degree and 1.5 cycles/degree. In view of the spatial tuning of visual neurones (e.g. see ref. 15), we assumed that these two spatial frequencies would probably activate different populations of visual neurones. Results from one of the cats tested in this first experiment appear in Fig. 3, which plots on log/log coordinates contrast increment thresholds as the function of background contrast. Each data point is the arithmetic mean of at least 8 threshold estimates. Open symbols show the results for the lower spatial frequency and filled symbols the results for the higher spatial frequency; the pair of error bars appearing on each set of data specify + 1 standard error, and the two members of each pair show the largest and smallest standard error for that condition. Across both conditions, standard errors averaged 9~o (i.e. less than 1 dB) of the mean. The two arrows along the ordinate denote the contrast thresholds for detection of these spatial frequencies in the absence of any background contrast. As already known, the cat is more sensitive (i,e. contrast threshold is lower) at 0.5 cycles/degree than at 1.5 c y c l e s / d ~ e e , which is why these two threshold values fall at different points along the ordinate. A least squares criterion was employed to fit a straight line to each set of increment thresholds. The slopes of these resulting lines are given in the figure inset. Clearly, the contrast discrimination function is steeper for the lower spatial frequency than it is for the higher one. This same pattern of
159
Stationary •
ll
.10
oo
J
-¢ .o~
J
o 0.5 c/d (.70) 0
•
1,5 c/d
(.-54)
Oe-
!
.~t DI
I
(~
. 3
I
I
I I I II
,10
I
I
.30
Background contrast
Fig. 3. Contrast discrimination functions for one cat at two spatial frequencies, 0.5 cycles/degree (open symbols) and 1.5 cycles/degree (filled symbols). Data points are the arithmetic mean of at least 8 threshold estimates, each obtained using a forced-choice staircase procedure. The error bars show + 1 S.E.M., and the pair of error bars shown for each function represent the largest and the smallest standard error for that condition. The arrows show contrast thresholds in the absence of a background grating. The slopes of the best fitting straight lines are given in parentheses within the inset. The correlation coefficient for the best fitting straight lines are 0.94 and 0.88 for the low and the high spatial frequency, respectively.
results was also found for the other cat (slope = 0.86 at 0.5 cycles/degree, with a correlation coefficient of 0.94; slope = 0.53 at 1.5 cycles/degree, with a correlation coefficient of 0.87).
Experiment 2 In the first experiment, a steady contrast increment was added to a steady background contrast to produce the grating of higher contrast. The contrast increment, in other words, contained no temporal modulation relative to the background. (Of course, the retinal image of the combined background and increment will undergo some degree of temporal modulation, owing to eye movements). One could argue, therefore, that this condition selectively activates neural mechanisms responsive to sustained contrast levels. We wondered whether contrast discrimination performance would change when the contrast increment consisted of a temporal modulation in contrast presented against a steady background level.
To answer this question, the following experiment was performed. In this second experiment, the contrast increment consisted of a sinusoidal modulation in contrast, whereby the increment was steadily introduced and removed at a fixed temporal frequency. Such a test stimulus can be considered as the sum of a steady grating (the background component) and an 'ON/OFF' flickering grating (the contrast increment). So, on each trial one CRT displayed the background component only while the other CRT displayed the background plus the temporally modulated contrast increment. The cat was reinforced for selecting the modulated contrast increment. As in the previous experiment, we measured contrast increment thresholds for different levels of background contrast. This was done for two rates of temporal modulation, 1.5 Hz and 8 Hz, at both 0.5 cycles/degree and 1.5 cycles/degree. Results from one Cat are summarized in Fig. 4. The left panel shows increment thresholds for the 1.5 Hz condition and the right panel the results for the 8 Hz condition; standard errors were comparable to those plotted in Fig. 3. Again, the bestfit lines reveal that contrast increment functions are steeper for the lower spatial frequency (slope values are given in parentheses within the figure). Also, for a given spatial frequency the function is steeper for the lower temporal frequency. This tendency is most pronounced at 1.5 cycles/degree, where thresholds for the 8 Hz contrast increment vary hardly at all with the background contrast. Complete functions were not obtained from the other cat, but selected points revealed the same trends as those seen in Fig. 4. DISCUSSION
The present results clearly show that the cat's ability to discriminate contrast increments depends upon the background contrast against which that increment is presented. In particular, increment thresholds increase with background contrast. Within the range of background contrast values studied, this relationship is adequately described by a straight line plotted on log/log coordinates. Contrast increment thresholds do
160
.50
I
1.5 hz
"
8 hz
.50
u'J 0 to ¢.)
.10
(.7o) o 0.5 c/d (.521 • 1.5 c/d
e,....~o~
4--
¢:
E
0
(.60) (.14)
o.lO /
.10
~ o /
0
t,.
co ¢-
-- .05
.05 I .05
I .10
I .50
Background
I
I
I
.03
.10
,50
contrast
Fig. 4. Contrast discrimination functions for one cat at two temporal frequencies, 1.5 and 8 Hz. The details are as in Fig, 3.
not increase as a constant proportion of the background (i.e. the slope of the contrast increment function is less than 1.0), thus indicating a departure from Weber's law. This departure is noteworthy, since evidence for Weber's law has been obtained in the cat on an increment detestion task where the display consisted of a large, circular spot of white light seen against a uniform background 13. This display could be construed as a low spatial frequency target appearing against an even lower (approaching zero) spatial frequency background. Considered together, these previous findings and the present results imply that the slope of the contrast increment function becomes steeper at lower spatial frequencies. The slope of the contrast discrimination function (as indexed by the slope of the best-fitting line in log/log coordinates) varies with spatial frequency, being steeper for the lower spatial frequency. Testing with temporally modulated contrast increments served further to exaggerate these differences between low and high spatial frequency gratings. This same pattern of results was found by Burbeck and Kelly7 in their study of contrast discrimination in humans. In their experiment, test and background patterns differed in orientation, but otherwise their procedures resembled those used in the present study. In other studies involving human observers, contrast
increment thresholds have been measured using briefly flashed grating p a t t e l ' n s !°,ll,16AT. Under those conditions, spatial frequency has minimal effect on the slopes of the resulting contrast discrimination functions - the resul~g slope values fall in the neighbourhood of 0:7, a value close to that found for the cat at 0.5 cycles/degree.
Physiological implications Are there response properties of cat visual neurones that might account for these behavioural findings? To address this question, several assumptions must be made concerning the nature of this contrast discrimination task. First, we assume that increases in background contrast produce a monotonic increase in the response amplitude of visual neurones. Ignoring saturation effects, this assumption is supported by physiological data 1,9"14, Second, we assume that increment threshold performance depends on a fixed, criterion difference between the response to the background alone and the response to the background plus increment. This is a fairly standard assumption in threshold studies. Now given these assumptions, let us consider possible physiological correlates of two aspects of the present findings, beginning with the departure from Weber's law. Physiological measurements have established that many cortical cells exhibit a compressive
161 non-linearity (e.g. see ref. 1). In other words, the slope of the function relating response to contrast becomes shallower at intermediate and high contrast levels. This means that to elicit a just discriminable increase in neural activity, larger increments in contrast are required at higher contrast levels. This neural response compression could underly the compressive nature of the contrast discrimination function. In fact, Albrecht and Hamilton I fotmd that in their large sample of cat cortical cells, the average slope of the contrast response function was 0.59; for purposes of comparison, the average of all the slope values for the contrast discrimination functions shown in Figs. 3 and 4 equals 0.54. Considering next the variation in the slope of the contrast discrimination function with spatial frequency, we have considered two possible explanations for this finding. First, it could be that a single neural mechanism underlies discrimination performance at all spatial frequencies and that the gain of this single mechanism (i.e. the growth of response with contrast) changes with spatial frequency. In fact, there is physiological evidence that individual cortical cells exhibit just such behavior, with each cell showing its greatest gain at the optimal spatial frequency for that cell9. However, this explanation does not fit well with other psychophysical evidence indicating that the cat utilizes different neural mechanisms when detecting spatial frequencies differing by an octave or more 5. Based on those findings, we would expect the cat to utilize that mechanism exhibiting the greatest contrast gain for the condition under test, a strategy yielding the largest number of correct choices. According to this second hypothesis; the cat, when tested at 0.5 cycles/degree, would utilize a different population of neurones than those utilized when tested at 1.5 cycles/degree. Is there physiological evidence for variations in contrast gain among different classes of visual neurones? Considering first cat retinal ganglion ceils, it has been reported that Y cells exhibit steeper contrast/response functions than do X cells 19. There is also evidence that Y cells are more responsive than X cells at lower spatial frequencies, while at higher spatial frequencies this tendency is re-
versed 8. (Incidentally, these physiological measurements were performed at light levels comparable to that used in our behavioural work.) So considered together, these physiological properties of X and Y cells imply that contrast discrimination should be better at low spatial frequencies (where the contrast/response function is steeper), which it is. However, this suggestive parallel between psychophysics and physiology disappears when we examine the response properties of striate cortex neurones. Among striate units, the steepest contrast/response functions are exhibited by those cells classified as 'special complex', but there is no tendency for this class of cortical cells to respond to lower spatial frequencies9. And there are certainly no clear differences between the contrast/response functions of simple cells and regular complex cells 2'9, the two cell types thought by some to be the cortical analogues of the retinal X and Y cells 2°. So at present, the evidence linking contrast discrimination to particular classes of visual neurones remains rather weak. Finally, Fig. 4 indicates that at 1.5 cycles/degree (a high spatial frequency for the cat) a stationary background grating has virtually no effect on the cat's ability to detect a contrast increment temporally modulated at 8 Hz. Evidently the neural mechanism mediating detection of the transient modulation in contrast is unaffected by the steady background. One might attempt to explain this lack of interaction between a transient stimulus and a steady one in terms of sustained and transient visual neurons, a dichotomy that has been popularized in recent theorizing. However, the absence of similar trends at the lower spatial frequency (0.5 cycles/degree) makes us cautious in advancing such an interpretation. ACKNOWLEDGEMENTS
This work was supported by grants from the National Institutes of Health (EY01596) and from the Alumnae Board of Northwestern University. We are grateful to Karen Holopigian, Karin Boothroyd, Gregory Phillips and Geoffrey Iverson for helpful discussion. I.P. is now at the University of Pittsburgh Medical School.
162 REFERENCES 1 Albrecht, D.G. and Hamilton, D.B., Striate cortex of monkey and cat: contrast response function, J. Neurophysiol., 48 (1982) 217-237. 2 Berkley, M.A., Visual discriminations in the cat. In W.C. Stebbins (Ed.), Animal Psychophysics: The Design and Conduct of Sensory Experiments, Appleton-CenturyCrofts, New York, 1970, pp. 231-247. 3 Bisti, S. and Maffei, L., Behavioural contrast sensitivity of the cat in various visual meridians, J. Physiol. (Lond.), 241 (1974) 201-210. 4 Blake, R., Cool, S.J. and Crawford, M.L.J., Visual resolution in the cat, Vision Res., 14 (1974) 1211-1217. 5 Blake, R. and Martens, W., Critical bands in cat spatial vision, J. Physiol. (Lond.), 314 (1981) 175-187. 6 Bloom, M. and Berkley, M.A., Visual acuity and the near point of accommodation in cats, Vision Res., 17 (1977) 723-730. 7 Burbeck, C.A. and Kelly, D.H., Contrast gain measurements and the transient/sustained dichotomy, J. Opt. Soc. Amer., 71 (1981) 1335-1342. 8 Cleland, B.G., Harding, T.H. and Tulanay-Keesey, U., Visual resolution and receptive field size: examination of two kinds of cat retinal ganglion cell, Science, 205 (1979) 1015-1017. 9 Dean, A.F., The relationship between response amplitude and contrast for cat striate cortical neurones, J. Physiol. (Lond.), 318 (t981) 413-427. 10 Legge, G.E., Spatial frequency masking in human vision: binocular interactions, J. Opt. Soc. Amer., 69 (1979) 838-847. 11 Legge, G.E., A power law for contrast discrimination, Vision Res., 21 (1981) 457-467.
12 Legge, G.E. and Foley, J.M., Contrast masking in human vision, J. Opt. Soc. Amer., 70 (1980) 1458-1471. 13 Loop, M.S. and Millican, C.L., Increment thresholds in normal and binocularly deprived cats, Behav. Brain Res.. 9 (1983) 143-150. 14 Maffei, L. and Fiorentini, A., The visual cortex as a spatial frequency analyser, Vision Res., 13 (1973) 1255-1267. 15 Movshon, J.A., Thompson, I.D. and Tolhurst, D.J., Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex, J. Physiol. (Lond.), 283 (1978) 101-120. 16 Nachmias, J. and Sansbury, R., Grating contrast discrimination may be better than detection, Vision Res., 14 (1974) 1039-1042. 17 Pantle, A., Simultaneous masking of one spatial sine wave by another, Invest. Ophthal. vis. Sci., Suppl. 16 (1977) 47. 18 Robson, J.G., Receptive fields: spatial and intensive representation of the visual image. In D. Carterette and W. Friedman (Eds.), Handbook of Perception, Vol. 5, Academic Press, New York, 1975, pp. 81-112. 19 Shapley, R.M. and Victor, J.D., The effect of contrast on the transfer properties of cat retinal ganglion cells, J. Physiol. (Lond.), 285 (1978) 275-298. 20 Stone, J. and Dreher, B., Projection of X- and Y-cells of the cat's lateral geniculate nucleus to areas 17 and 18 of visual cortex, J. Neurophysiol., 36 (1973) 551-567. 21 Swanson, W.H., Wilson, H.R. and Giese, &C., Contrast matching data predicted from contrast increment thresholds, Vision Res., 24 (1984) 63-75. 22 Wetherill, G.B. and Levitt, H., Sequential estimation of points on a psychometric function, Brit. J. math, stat. Psychol., 18 (1965) 1-10.