Vision Ra.

Vol. 17. pp. 1057 to 1065. Pergamon

SPATIAL

Press 1977. Printed in Great

Britain

FREQUENCY ADAPTATION CAN ENHANCE CONTRAST SENSITIVITY KAREN K. DE VALOIS

Primate Vision Laboratory, Psychology Department, University of California, Berkeley, CA 94720. U.S.A. (Received 18 October 1976; in revised form 2 February 1977) A~~ct-Adaptation to a high-contr~t sinusoid& ium~nan~ grating produces a temporary, bandlimited loss in sensitivity centered around the adaptation frequency. The decrease appears to be both narrower and more symmetrical than earlier reports suggest. The effect falls to zero by f f 1 octave and is not reliably present from f f 1 octave to f k 2 octaves. Enhancement of contrast sensitivity occurs for frequencies further removed. peaking at about f + 2f to 3 octaves. This suggests mutual inhibitory interactions among spatial-frequency-selective units of varying filter characteristics. Longterm practice produces significantly higber contrast sensitivity functions and narrower bandwidths of the a~p~tional ~n~ti~ty loss. Key Words--adaptation;

contrast sensitivity; enhancement.

Adaptation to a high-contrast sinusoidal luminance grating produces a temporary depression in the contrast sensitivity to gratings within a restricted hand of spatial frequencies (Mantle and Sekuler, 1968; Blakemore and Campbell, 1969). The sensitivity loss can be produced by gratings of a wide range of spatial frequencies, is centered on the adaptation frequency, and falls to zero at about f 5 1 octave. The effect is orientation specific (Gilinsky, 1968) and shows partial interocular transfer (Blakemore and Campbell, 1969), thus suggesting that it is cortical in origin. This adaptation effect has been taken as evidence for multiple separate channels in the visual system, each of which is responsive to a limited range of spatial fre-

quencies. Arguments for the functional independence of these spatial-frequent channels are based on the following facts: the contrast threshold for any of several complex waveforms is determined solely by the contrast threshold of the waveform’s fundamental Fourier component (Campbell and Robson, 1968); sine waves and square waves of the same (high) frequency are indiscriminable at threshold, and square waves become dis~iminable from sine waves only when their third harmonic components reach their individual contrast thresholds (Campbell and Robson, 1968); and the presence of a second subthreshold grating does not affect the contrast required for the detection of a gratingf unless the second grating has a frequency within the range of 4j5 to 5/4f (Sachs, Nachmias and Robson, 1971). (If the second grating is within that frequency range detection is facilitated, suggesting that the two gratings might be exciting overlapping classes of detectors.) On the other hand, the contrast threshold of a grating f can be significantly increased by the presence in the field of a suprathreshold grating of another frequency (Pantle, 1974). Also, in recordings from frequency-selective cells in the striate cortex of macaque monkeys, it has been found that the presence in the receptive field of a suprathreshold grating of frequency

4f (to which a cell gives no response

it is presented alone) can reduce the amplitude of the cell’s response to a gratingf to which it is most sensitive (De Valois, Albrecht and Thorell, 1977). The latter two types of experiments suggest that frequencyselective channels are not functionally independent. Other psychophysical studies have also suggested that spatial frequency channels are not truly independent. Tolhurst (1972) and Nachmias, Sansbury, Vassilev and Weber (1973) have shown that the loss in sine-wave contrast sensitivity following adaptation to square-wave gratings is not precisely predictable from the behavior of each component frequency in isolation. Following adaptation to a suprathreshold squarewave grating (or even to a mixture of two sinusoidal gratings with 3: 1 frequency ratio), the loss in contrast sensitivity is not as great as one would expect from a truly linear system. Tolhurst (1972) suggests that this is due to ~hibito~ interactions among spatial frequency channels subserving the first and third harmonics when those frequency components are suprathreshold. Additional evidence suggesting inhibitory interactions among channels has been provided by Stecher, Sigel and Lange (1973), Dealy and Tofhurst (1974) and Henning, Hertz and Broadbent (1975). This study approaches the question of independence of channels by extending the adaptation paradigm used by Blakemore and Campbell (1969) to examine the effect of adaptation on frequencies far removed from the adaptation frequency. In the course of the experiment, a considerable amount of data was obtained relevant to the frequency-specific adaptation effect. While the principal findings of Blakemore and Campbell (1969) were amply confirmed, there were a number of disagreements with respect to other aspects of the effect.

METHOD Apparatus The stimuli in this experiment were sinusoidal luminance when gratings produced on a Tektronix 602 oscilloscope with 1057

105x

KAREN K. DE VALOIS

a P4 white phosphor. Details of the circuitry are reported elsewhere (De Valois. 1977). During trials. subjects could adjust the contrast of the grating by means of a ten-turn potentiometer set to any of six sensitivity ranges, In the early stages of the experiment a linear potentiometer was used. A logarithmic potentiometer was substituted during the latter stages. No reliable differences were produced by the substitution. Stimuli were generated by a Data General Nova 1220 computer, which presented the trials and adaptation periods, and recorded. analyzed, and printed out the data at the end of each session. Procrdurr

Subjects were seated in a darkened room, with their heads immobilized by a chin and forehead rest, 85 cm from the oscilloscope face. Observations were monocular, and stimuli were viewed through a 2 mm artificial pupil. The oscilloscope was seen through a rectangular aperture subtending 4.3 x 5.5” visual angle in a white s’creen subtending 71 x 56’. The screen was front-illuminated so that its luminance approximately matched the unvarying mean luminance of rhe stimulus pattern, which was 0.43 cd/m2. (This luminance was chosen to match the stimuli used in another experiment being run concurrently.) During the pre-adaptation period the gratings of various spatial frequencies were presented to the subject in a random order. The subject adjusted the contrast of each until he was satisfied with his threshold setting, then pushed a button which caused the computer to record his potentiometer setting and present the next stimulus. Stimuli were luminance-modulated sinusoids which covered the frequency range from 0.59 to 22.63 c/deg in 114 octave steps. After settings had been completed at all 22 frequencies, a preselected adaptation frequency was presented at maximum contrast (95%) for 5 min. The grating was steady and did not drift. Subjects were instructed to scan the adaptation pattern with a constant circular motion to prevent the formation of conventional afterimages. Two seconds before the end of the adaptation period a warning bell sounded. The adaptation stimulus was then replaced by a test grating. If at the end of 5 set the subject had not completed his response the adaptation grating was again presented for 10 sec. Subjects were allowed as many stimulus presentations as necessary to make a setting at any frequency. Once a response was completed, the adaptation grating was presented again for 20sec. then followed by the next stimulus frequency. Stimuli were presented in the same (random) order both before and after adaptation. The adaptation gratings used ranged in frequency from 0.84 to 13.45 c/deg. A minimum of three sessions were run at each adaptation frequency for two of the three Ss. Much more extensive data were collected for adaptation at two frequencies, 1.19 and 8.00 c/deg, respectively. These frequencies were chosen in order to show facilitation at both higher and lower frequencies. In each case, the test frequencies ranged from at least f f 1 octave to .f k 3 l/2 octaves. For these two frequencies data were also collected over a period of almost 12 months, with replications being carried out at approximately six month intervals to examine long-term changes in the effects with time and practice. Subjects

Three subjects were used. The most extensive data were collected from subiect RDG. who had never before been a subject in any experiment and knew nothing of the aims or results of this experiment until it had been completed. He was myopic, with his acuity corrected to 20/20 by the use of spectacle lenses placed just beyond the artificial pupil. KDeV and RDeV had both served as subjects in previous vision experiments. Both were aware of the aims and ongoing results of the study. Neither had significant refractive error.

RESULTS

A convenient way to present the various etfects of spatial frequency adaptation is to examine separately the changes at various distances from the adapting frequency. This is what we do here. f f 1 octnav Adaptation at any frequency 1‘ produced a marked decrease in contrast sensitivity for a restricted band of spatial frequencies, as discovered by Blakemore and Campbell (1969). They reported that at high spatial frequencies this sensitivity loss was centered on the adaptation frequency, but that for adaptation frequencies below 3 c/deg the effect was centered at 3 c/deg. This study, like that of Jones and TulunayKeesey (1975), did not confirm that finding. Rather, we found that the loss of sensitivity was always centered on the adaptation frequency, down to the lowest frequency used. 0.84c/deg. The discrepancy, as suggested by Jones and Tulunay-Keesey (1975), may be explained by the insufficient number of cycles present at low frequencies in the small field (1.5.) used by Blakemore and Campbell (I 969). The bandwidth of the sensitivity loss at half amplitude (calculated by the method of Blakemore and Campbell, 1969) averaged about 0.65 octave in this study, considerably narrower than that reported by Blakemore and Campbell (1969). The loss fell to zero at about f _+ 1 octave. Figure 1 shows contrast sensitivity before and after adaptation averaged over 11 sessions of adabting to a grating at l.l9c/deg for subject RDG. In Fig. 2a the adaptation effect is plotted by the method of Blakemore and Campbell (1969). The logarithms of the pre- and post-adaptation contrast sensitivities

I.0

27 .8

. pre adaptation . pDstadaptation

J+-_-_2

Spatial

4

Frequency

6

16

32

(c/deg)

Fig. 1. Log contrast sensitivity before (A) and after (0) 5 min adaptation to a 1.19 c/deg sinusoidal grating for subject RDG. Spatial frequency is plotted on the abscissa on a logarithmic scale. Hatch marks denote octaves. Each point represents the mean setting averaged over 11 sessions.

to59

Spatial frequency adaptation

lb)

2

_-----___

.c

II z.

E co v

.Ol I

Spatial

2

4

6

I6

32

Frequency (c&g)

2 -.I0

---

--___

-

-

s = -.20 I

Spotiol

2

4

Frequency

6

16

32

k/deg)

Fig. 2. Mean change in contrast sensitivity after adapting to 1.19 c/deg sinusoidal grating. Subject: RDG; n = 11 sessions. Dotted lines indicate significance levels (0 + 20) for redetermining contrast sensitivity after adaptation to a blank field (n = 4). (a) Relative threshold change plotted by the method of Blakemore and Campbell (1969). The ordinate represents the ratio of contrast sensitivity before and after adaptation, minus 1. Since negative values cannot be plotted on the logarithmic scale, they have been changed in sign and plotted as positive numbers. Negative values (showing an increase in contrast sensitivity) are represented by open circles; positive values (showing a decrease in contrast sensitivity) by filled circles. (b) The same data are replotted by simply showing the mean change in log contrast sensitivity. Since post-adaptation values are subtracted from pre-adaptation values, positive numbers show a sensitivity loss and negative numbers show a sensitivity increase. Since the logarithms of contrast sensitivities are used to calculate the differences, the effect on the mean of occasional abnormally large differences is reduced. This accounts for the apparent discrepancy in the direction of the function between the points at 1.68 and 2.OOc/deg and the fact that the positive portion of (2b) is not a simple monotonic transform of the same portion of (Za). were plotted, and the antilog of the difference between the two log contrast sensitivities was then taken (which gives the ratio of the actual scores). Since no change would give a ratio of 1, 1 was subtracted from each ratio in order to express the sensitivity loss as a positive increment above zero. If, with this procedure, one always subtracts post-adaptation scores from pre-ad+ptation scores, negative values cannot be plotted (on the logarithmic scale) since they fall below zero. But if one simply takes the absolute difference on the log scale, negative and positive scores cannot be discriminated. This was done in Fig. 2a. Since Blakemore and Campbell (1969) did not report any significant negative values this raised no difficulty. In this study, however, significant negative values were obtained, so the data have been replotted in Fig. 2b by subtracting the logarithm of the post-adaptation score at each frequency from that of the pre-adaptation score. The difference between the logarithms is then plotted on a linear scale as a function of fre-

1When a linear constant is subtracted from a function which is subsequently plotted on a logarithmic scale, large and small numbers will be differentially affected. The subtraction of a linear constant will have a much greater effect on the position of a small number on the logarithmic scale than on the position of a large number, due to the logarithmic compression of larger numbers. Thus, by subtracting 1 from the ratio of contrast sensitivities before and after adaptation, the formula used by Blakemore and Campbell produces a greater reduction in small numbers than in large numbers, thus narrowing the bandwidth of the function

quency. A loss in sensitivity will thus give a positive difference, and an increase in sensitivity, a negative difference. It should be noted that bandwidths calculated by

these two methods will not be identical. The procedure used by Blakemore and Campbell (1969) yields smaller estimates.’ For ease of comparison the bandwidths reported in this paper have been calculated by that method unless otherwise specified. (The term bandwidth here refers to full bandwidth at half amplitude.) Blakemore and Campbell (1969) calculated the average standard error for redetermining contrast sensitivity without adaptation, took the ratio of twice the standard error of the difference to the original mean, and plotted it on the ordinate as a measure of significance. I have taken the average standard error of re-determining contrast sensitivity after adapting to a blank field as being a somewhat better measure since it allows for the effects of time in the test situation and the different sequence of events in the pre- and post-adaptation periods. (As always, the test grating was on continuously during the pre-adaptation period but was on for only 5 out of every 15 set during the post-adaptation period. The intervening 1Osec were, in these control sessions, filled with a blank field. Thus any systematic difference between pre- and post-adaptation measures due to the different sequence of events should have been revealed by these control sessions.) For subject RDG this standard error (taken over four sessions) is 0.024 log units. If one takes twice the standard error, 0.048, then takes

1060

KAREN K. DE VALOIS

its antilog and subtracts 1 so it can be plotted on the ordinate of Fig. la. a significance level of 0.115 is obtained. Since the actual difference between the logarithms of the pm- and post-adaptation scores is plotted on the ordinate in Fig. lb. a corresponding significance region can be indicated by zero _t twice the standard error for redetermining contrast sensitivity with adaptation to a blank field. This level is shown by the dotted lines at iO.048 on the ordinate. As can be seen, the adaptat~ona1 loss in the region of ,f‘F 1 octave far exceeds this error range. f I I-2 octavrs In the region off & l-2 octaves no reliable change from the pre-adaptation contrast sensitivity was found, as can be seen in Fig. 5. This was often more apparent in the data from individu~ sessions, when the pre- and post-adaptation contrast sensitivities were often identical within a region of l-l l/2 octaves between the depression centered around the adaptation frequency and the facilitation at frequencies farther removed. Figure 3 shows an example of this with data from one session for subject RDG. The adaptation frequency was 1.19 c/deg. Each point reflects the difference between one pre- and one postadaptation setting.

As the difference between adaptation and test frequencies increased beyond 2 octaves, the post-adap tation contrast sensitivity became significantly higher than the pre-adaptation measures for the same frequency. Detection of gratings was facilitated rather than depressed by the prior adaptation. This facilitation generally reached its maximum at f +_ 2 l/2 octaves or beyond. The bandwidth of the facilitation at half-amplitude averaged about 0.60 octave. The maximum amplitude of the facilitation varied considerably (though not predictably). It was on the average about l/3 of the amplitude of the sensitivity loss at Sand rarely exceeded l/2 of that amplitude. (Since adaptation was carried out at the same contrast level,

Spatial

Frequency

(c/degl

Fig. 3. An example of data from a single session. Subject: RDG: adaptation frequency: 1.19 c/deg. Note the extended region of no adap~tional change, covering, here, 1 3/4 octaves between the primary adaptation effect and the facilitation at frequencies further removed.

f

il

$2

t3

t4

Spatial Frequency in Octaves (Relative to the adaptation Frequeocy)

Fig. 4. Change in log contrast sensitivity as a function of spatial frequency in octaves relative to the adaptation frequency, irrespective

of direction.

Twenty-two

sessions.

using two adaptation frequencies (11 at 1.19c/deg.: I1 at 8.OOc/deg),were combined with all measurements at a given distance (e.g. f 1 octave) being averaged together. For subject RDG, 0 + 0.048 encompasses the region of 0 f 2u for change in log contrast sensitivity following adaptation to a blank field. Note the linear fall-off of the primary adaptation effect. 95x, regardless of frequency, the amplitude of the sensitivity loss varied somewhat with frequency, as reported by Blakemore and Campbell, 1969.) The shape of the function can be seen in Fig. 4. Data were averaged from 11 sessions at each of two adaptation frequencies, 1.19 and S.oOc/deg, for subject RDG. Change in contrast sensitivity is plotted as a function of the difference in octaves between the adaptation and test frequencies irrespective of direction, since facilitation occurred for test frequencies both lower and higher than the adaptation frequency. The maximum facilitation is seen here at f +- 2 3/4 octaves, Figure 5 presents data From three Ss averaged over 59 sessions with adaptation frequencies ranging from 0.84 to 13.45 c/deg. Data were aligned on the abscissa so that the adaptation frequencies coincided, and means were calculated for each l/4 octave step away from the adaptation frequency. Although it appears from these data that faciIitation was ~nsiderably greater when the test frequency was lower than the adaptation frequency, that was not invariably true. In fact, for one subject, RDG, the reverse was quite consistently the case. Neither KDeV nor RDeV, however, showed such a predictable relationship.

Two of the subjects in this study, KDeV and RDG, were run in either this experiment or closely related tasks almost daily over a period of 1.5 yr. We therefore have data which show the long-term changes in performance on these tasks with practice. Two points of interest are apparent. The first concerns the absolute increase in cOntra.st ~nsitivity over time. Figure 6 presents three determinations of the luminance con-

___ -_4 1061

Spatial frequency adaptation

-4

-3

-2

Spatial

-I

!

Frequency

I

in

lRelotive lo the adoplotion

2

3

4

Octaves Frequency)

Fig. 5. Change in contrast sensitivity as a function of spatial frequency in octaves relative to the adaptation frequency. Measurements were made at l/4 octave intervals. Data collected from three subjects in 59 sessions were averaged after normalizing for adaptation frequency.

trast sensitivity function for subject RDG. The first (n = 3) was based on data collected in August/September, 1975. At this point RDG was already a practiced and highly reliable subject, having been a subject in similar experiments for 6 months. The second determination (n = 4) was based on data collected about six months later, February, 1976. The third function (n = 4) is based on data collected in August, 1976. Although these three functions represent discrete periods, data were collected during the entire year. The increase in contrast sensitivity occurred gradually without obvious steps.

I.0

0.1

Spgtial

Frequency

10.0

Mdeg)

Fig. 7. Relative threshold increase (plotted by the method of Blakemore and Campbell, 1969) following adaptation at 1.194deg. Open circles represent data from three sessions run approximately a year before the four sessions which supplied the data represented by filled circles. The subject, RDG, had run almost daily sessions on similar or identical tasks during the intervening months. Note the significantly greater amplitude and narrower bandwidth (0.69 octave as opposed to 0.94 octave) of the more

recently-collected data.

The second point of interest concerns the change in the adaptation effect over time. The bandwidth of the primary adaptation effect decreased significantly. At the same time, its amplitude often (though not invariably) increased. An example of this change can be seen in Fig. 7, showing two sets of data from subject RDG with adaptation at 1.19 c/deg. The bandwidth at half amplitude of the earlier function is 0.94 octave. That of the later function is 0.69 octave. RDG showed a similar decrease in the bandwidth of the adaptation effect when an 8.OOc/deg adaptation stimulus was used. The bandwidth at half amplitude decreased, in this case, from 0.78 to 0.65 octaves 6 months later to 0.40 octaves following another 6 months. The amplitude of the facilitation generally increased considerably, also, although it is not obvious in this example. Variability of settings, either pre- or post-adaptation, did not change significantly over the 1Zmonth period. DISCUSSION

,

I I

2

Spatial

4

8

Frequency

b

I6

, 32

(c/deg)

Fig. 6. Three unadapted contrast sensitivity functions for one subject (RDG) taken at approx 6-month intervals. The earliest function is based on three sessions. The two subsequent functions are based on four sessions each.

The primary implication of this study is that the spatial-frequency-selective channels of the human visual system are not independent. They appear to be tonically in a mutually inhibitory relationship such that the adaptation (and consequent reduction in sensitivity) of one channel or group of channels is accompanied by an increase in sensitivity of another channel or group of channels. Detection of certain spatial frequencies is therefore facilitated by adapting to certain other spatial frequencies.

106’

Spatial frequency adaptation

The customary explanation of the spatial-frequency adaptation effect is that prolonged exposure to a high-contrast grating (and thus prolonged excitation) produces a temporary loss of sensitivity in those detectors which are particularly responsive to the adaptation grating. The results of this experiment suggest that those units not only are excited by a grating of the adaptation frequency. but that they also inhibit other units which are most sensitive to other frequencies. When the first group of units is adapted, then, not only their sensitivity but also their inhibitory effects are reduced. Thus the previously inhibited units are released from their inhibition and show an increased sensitivity to the frequencies to which they are responsive. It is of interest to note that facilitation has rarely been reported in studies of the spatial frequency adaptation effect. In fact, Barlow, Macleod and van Meeteren (1976) have questioned whether it is possible to show any compensatory advantage following spatial frequency-specific adaptation. The most comprehensive study, that of Blakemore and Campbell (1969), specifically states that no significant negative values-i.e. facilitation-were found. However, no data were reported for frequencies further removed from the adaptation frequency than 1: octaves, while the facilitation seen here is greatest in the region of 253 octaves. Barfield (1976), on the other hand, carefully examined the effect of adapting at f on the contrast sensitivity to 31: Using a two-alternative, temporal forced choice procedure she found a facilitation of about 0.125 log units at the third harmonic, but no consistent effect at the fifth harmonic. She also noted that the reports of Nachmias et u/. (1973) and Graham (1972) suggest that they also saw slight facilitation at the third harmonic. Barfield suggests that Blakemore and Campbell (1969) failed to find facilitation because of their psychophysical technique, the method of adjustment, and interference from the “illusory gratings” described by Georgeson (1976). I would suggest rather that they failed to find it because they did not measure frequencies beyond the fourth harmonic. In the region of f k l---2 octaves (the third harmonic is ,f + 1.59 octaves) facilitation does not reliably occur. Although it is often present. it is small (as Barfield found) and inconsistent. Of those studies which have examined the effect of adaptation on frequencies beyond f + 1 octave, only Barfield (1976) has reported testing a frequency more than two octaves removed from the adaptation frequency. She found that measurements at the fifth harmonic did not consistently show’ significant facilitation. This contradicts the data reported here, which suggest that the magnitude of the facilitation reaches its maximum beyond two octaves (the fifth harmonic is equivalent tof + 2.33 octaires). The details of Barfield’s study have not been published. so one cannot make direct comparisons. It is possible, however, that Barfield failed to see fifth harmonic facilitation because of the adaptation frequency used, 4.25 c/deg. For this frequency, the fifth harmonic is 21.25 c/deg, a frequency to which we are quite insensitive. The presumed small number of units tuned to this high frequency are perhaps not sensitive enough or sufficient in number to reflect the disinhibitory effect (if, in fact, it occurs at such high frequencies).

The most direct comparison with Barfield’s experiment from the data reported here is that for sessions in which we used an adaptation grating of 4.00 cjdeg. The highest test frequencies used were 19.03 and 22.63 c/deg. Never, in any session with any adaptation frequency, did the maximum facilitation occur at 22.63 c/deg and only occasionally at 19.03 c:‘deg. In eight sessions in which a 4.00 c/deg adaptation grating was used, the maximum facilitation occurred once at 19.03 c/deg, twice at 16.00 c/deg, once each at 9.51. 1.19, and 1.00 c/deg, and twice at 0.59 c/deg. This is a particularly confusing frequency range in which to adapt because it is near the transition point at which the maximum facilitation switches from higher to lower frequencies. When f = 4.00 c/deg, the range of f + 2 l/2-3 octaves is in the frequency regions to which we are least sensitive at both ends of the frequency spectrum, and large, reliable effects are not regularly seen. Although there is a fair amount of session-to-session variability in the point at which the maximum facilitation occurs, one common and perhaps rather surprising characteristic is that it generally does not occur at frequencies immediately adjacent to the primary adaptation effect. There is often a flat region of little or no change in contrast sensitivity between the depression centered about the adaptation frequency and the facilitation centered at some point generally more than two octaves removed. If one assumes that the facilitation is the result of disinhibition (or more strictly speaking, release from inhibition) between mutually inhibitory units, then one might expect the maximum facilitation to occur closer to the adaptation frequency. There are many examples of tonic mutual inhibition between units (Ratliff. 1965). In these, inhibition is generally greatest between units which are contiguous (or at least very close) along some dimension. In the case of frequency-tuned units, then, one might well expect maximum inhibition between units tuned to neighboring-+r at least very close-frequencies. The fact that facilitation occurs maximally between frequencies which are quite far removed suggests at first glance that this is not the case in the spatial frequency domain. If all units had a bandwidth at half amplitude of 1 octave, say, and their sensitivity fell to zero by f’ & 1 octave, then WC should expect that facilitation would appear immediately in the next frequencies with its maximum being centered at frequencies no further removed than ,f -i_ 2 octaves, and probably considerably closer. The units which would be maximally disinhibited would be those whose characteristic frequencies were closest to the adaptation frequency but which were not excited by the adaptation frequency to any substantial degree. The fact that this rarely occurs, however, is not surprising if one considers the actual bandpass characteristics of units in the visual system. In area 17. as well as at earlier levels, in both cat and monkey, single cells have been found to show differential frequency tuning. The characteristic frequency (i.e. the frequency to which a cell responds most vigorously and with greatest sensitivity) varies from cell to cell. It has also been found that breadth of tuning (i.e. bandwidth) varies substantially among cells. over a range of 0.5 to >2.5 octaves in the cat (Thorell and Albrecht, in preparation) and 0.7 to >2.5 octaves in

Spatial frequency adaptation monkey (De Valois et al., 1977). These large differences in bandwidth may occur in celis all of which have the same ch~a~~sti~ frequency, The diversity of channei bandwidth estimates obtained from psychophysical studies in humans suggests that there may be a similar range of bandwidths present in human visual cells, and that different psychophysical procedures may differentially assess them (Sachs et al., 1971; Blakemore and Campbell, 1969). Such a diversity of unit b~dwidths could also account for the finding that facilitation appears maximally at varying points, but almost always some distance away (on a frequency scale) from the primary adaptation effect. Assume that there are many units tuned to any given frequency and that those units have a variety of bandwidths. If each unit is mutually inhibitory with other units which are tuned to different frequencies and whose sensitivity regions abut but overlap only slightly or not at all, then frequency-specific adaptation would maximally depress sensitivity in cells which were tuned to the adaptation frequency, but significant disinhibition would occur in units tuned to a variety of frequencies, some very near and others far removed from the adaptation frequency. Some general predictions can be made if we assume that the visual system is somehow pooling the responses of all or most of the cells which respond to a given pattern. Since most cells tuned to frequencies near the adaptation frequency would be excited (and therefore subs~uently depressed in sensitivity), there would be a net loss in sensitivity for a region surrounding the adaptation frequency. Since most cells which are responsive to frequencies far removed from the adaptation frequency would not have been excited by the adaptation frequency but rather released from inhibition by other cells with which they are mutually inhibitory (and which had been adapted), there would be a net increase in sensitivity at those frequencies. At intermediate frequencies, however, these two factors might be expected to cancel each other, producing no net change in sensitivity. If, however, the visual system is detecting on the basis of the single most sensitive unit at any given frequency or for any particular pattern, then looking at the pooled responses of large numbers of cells would give us very little information. If that were the case, the location of the maximum facilitation at frequencies far removed from the adaptation frequency would suggest that inhibition occurred maximally between units which were not contiguous but, rather, far removed on the frequency scale. Primary adaptation

effect

Although this study confirmed the major findings of Blakemore and Campbell (1969), some points of difference should be noted. In their discussion of the spatial frequency adaptation effect, Blakemore and Campbell attempted to fit their data by the function [e-/ - ee12X)2]2.The part of this expression describing the high-frequency end of the curve is quite similar to the function y = Ae”‘/* used by Campbell, Cooper and Enroth-Cugell (1969) to describe the high-frequency fall-off in sensitivity of single units in cat LGN and cortex. The same function also describes quite well the hip-frequency fall-off in sensitivity of some monkey geniculate and cortical C&S

1063

(De Valois et al., in preparation). However, if the psy chophysical adaptation function were a reflection of the sensitivity profile of such cells, and if the reduction of sensitivity after adaptation were proportional to their unadapted sensitivity to the adaptation frequency, then the assymetry should be reversed-i.e. the fall-off should be more rapid at the low-frequency end, with a gradual tapering off at high frequencies. As Stromeyer and Klein (1974) have noted, the shape of the adaptation function should be a left-right inversion of the sensitivity profile of the underlying detectors. The use of a single expression to describe the characteristics of spatial frequency channels fails to take into account the enormous variety of shape and breadth of tuning found in single units. If the channel being revealed by spatial frequency adaptation is composed of many different single units whose activity is somehow summed or averaged, then one cannot predict the characteristics of the channel from the responses of one cell unless all the cells are identical. Since that clearly is not the case, and since we do not have sufficient information about the distribution of cell characteristics in the population, we cannot predict the characteristics of the channel from the available recording information. Thus there is no particularly compelling theoretical reason to expect that the psychophysical adaptation function should be so similar to the physiologically derived function for individual cells. The data collected in this study do not even approximate the function [edS” - e-(2/)*]2 which Blakemore and Campbell (1969) have fitted to their data. The primary adaptation effect is almost invariably narrower and more symmetrical than those described by Blakemore and Campbell. The average bandwidth of the s~sitivity loss (when plotted after the method of Blakemore and Campbell) was only about 0.68 octaves, averaged over 59 sessions. The bandwidth of the effect was often considerably narrower when results from just one adaptation frequency were plotted, although there was no systematic variation with adaptation frequency. (Very high adaptation frequencies were not used.) Figure 8 shows data from all three subjects plotted against the theoretical function used by Blakemore and Campbell (1969). In each case, the data represent all the sessions run by each subject. (The averaging was carried out on measures of log contrast sensitivity. These functions were then converted to the scale used by Blakemore and Campbell.) All four curves are normalized on both the abscissa and the ordinate so that the measure of the effect at the adaptation frequency overlies the maximum of the theoretical function. The reason for this difference is not clear. There are several procedural differences between the two experiments which could conceivably account for part or all of the differences of effect. For example, Blakemore and Campbell used a 1.5” circular field as opposed to the 4.3 x 5.5” rectangular field used here. They used an on-off flashing stimulus, while gratings in our experiments were steady; and they limited adaptation time to 1 min, while we used 5 min adaptation periods. I have replicated all these conditions singly and in combination without significantly in-

IOh4

KAREN K. DE VALOIS

i i. \ * - KDeV *-RN’ A-RDG

0.01 I I

Spatial

2

4

Frequency

8

16

icldegl

Fig. 8. Relative threshold elevation averaged over many sessions for each of three subjects. Data have been norma-

lized on the abscissa so that all adaptation frequencies overlap at 3.36c/deg and normalized on the ordinate so that the peak amplitudes are all identical to the peak of the function [e-/’ - e -“‘J2 represented by the heavy line. Note that all three data functions are both narrower and more symmetrical than the theoretical function. creasing the bandwidth of the effect. The oniy noticeable difference produced was a general increase in variability when all three conditions were changed to those used by Blakemore and Campbell. The other major difference between the procedure used by Blakemore and Campbell (1969) and that used in this study was that of mean lu~n~ce level. Blakemore and Campbell used a mean luminance level of approx 100cd/m2, while the luminance level in our experiments was 0.43 cd/m’. It is not immediately obvious why such a difference in luminance should produce a difference in bandwidth but we hope to test its effect as soon as possible. A more likely expl~ation for the different may lie in the number of sessions run. It is not clear from their description just how many times Blakemore and Campbellrepeatedadaptationateachfrequency, but the lack of discussion and the viability of the functions suggest that there were not many sessions run. The absence of change in the contrast sensitivity function between the beginning and the end of the experiment also suggests that only a short time elapsed. The data reported here are based on many sessions for each subject, and two of the three subjects were quite experienced in similar visual tasks before the experiments began. The data were collected in a series of almost daily sessions over a period of a year and a half for two of the three subjects, so we have a long-term baseline with which to compare data collected over a short period. One trend we have noted is a shift over time towards adaptation effects which are greater in amplitude but narrower in shape. Figure 7 shows an example of such a change. It is interesting to note the differences in the bandwidths of the three individual functions in Fig. 8. The largest

bandwidth, that of subject RDeV, is 0.85 octaves. RDeV ran considerably fewer sessions than either of the other two subjects. Although he had participated as a subject in many earlier visua1 experiments, he had not served as a subject in experiments similar to this one. KDeV and RDG had both served 3s suhjects in earlier phases of this study using color-varying gratings. Both were well”~racticed before the first of these data were collected, and both participated in many more sessions than did RDeV. The b~~ndwidtlls of their average adaptation functions were tt.hZ and 0.65 octaves for KDeV and RDC;. respectively. Whether the narrowing of the adaptation effect represents a criterion shift or an actual sensitivity change is not clear. If the data of Blakemore and Campbell (1969) were collected relatively quickly and over a short time period, then their broader adaptation effects may simply reflect this. A simple explanation of an increase in amplitude of the adaptation effect would be that subjects changed the part of the 5 set test interval in which they made their judgments. The earlier in the intervat the judgment was made, the greater should be the amplitude of the effect. However, this would explain neither the narrowing bandwidths nor the increase over time in unadapted contrast sensitivity (since those settings were made without time limits). The decreasing spread and often increasing amplitude of the adaptational effect might be explained if one assumes that detection is based on a pooled response of many cells which differ in their characteristic frequencies and bandpass characteristics. If, with increasing practice, a subject simply becomes more efficient at restricting the sample pool to those cells which are most sensitive to the frequency being observed, then one might expect that the amplitude of the adaptation effect would increase. If those cells are also narrower in their sensitivity range, then the bandwidth of the effect should also decrease. This would be, in essence, selectively attending to different types of detectors. Another possibility would be a change over time in the sensitivity profiles of the detectors involved, or perhaps the establishment of new connections between existing units. In either case, the change in the adaptation effect and the general increase in the contrast sensitivity function over time suggest that psychophysical experiments such as this one and those discussed earlier in this paper cannot be taken as simple, direct reflections of a simple, unvarying, underlying physiological organization. Acknow2rdgemPnrs-This research was supported by USPHS Grant No. EYOO014 and NSF Grant No, GB43289X. REFERENCES Barfield L. P. f1976)

Interaction in the human visual SyStern between sinusoidal gratings of harmoni~lly related spatial frequencies. J. Physiol.. Lond. 254. 67P-685’. Barlow H. B., Macleod D. 1. A. and van Meeteren A. (1976) Adaptation to gratings: no compensatory advantage found. Vision Res. 16, 1043-1046. Blakemore C. and Campbell F. W. (1969) On the existence of neurones in the human visual system selectively sensitiveto the orientation and size of retinal images. .I. Phtb siol.. Lmd. 203. 231-260.

Spatial frequency adaptation Campbell F. W., Cooper G. F. and Enroth-Cugell C. (1969) The spatial selectivity of the visual cells of the cat. J. Physiol., Land. 203, 223235. Campbell F. W. and Robson J. (1968) Application of Fourier analysis to the visibility of gratings. J. Physiol., Lond. 197, 551-566. Dealy R. S. and Toihurst D. J. (1974) Is spatial adaptation an after-effect of prolonged inhibition? J. Physiol., Lond. 241, 261-270. De Valois K. K. (1977) Independence of black and white: phase-specific adaptation. Vision Res. 17, 209-215. De Valois R. L., Albrecht D. G. and Thorell L. G. (1977) Spatial tuning of LGN and cortical cells in monkey visual system. In Spatial Contrast, Spekreise H. and van der Tweel H. (Eds.), Else~er~orth-Holland Press, Amsterdam. Georgeson M. A. (1976) Psychophysical hallucinations of orientation and spatial frequency. Perception 5, 99111. Gilinsky A. (1968) Orientation-specific effects of patterns of adapting light on visual acuity. J. opt. Soe. Am. 58, 13-18. Graham N. (1972) Spatial frequency channels in the human visual system: effects of luminance and pattern drift rate. Vision Res. 12, 53-68. Henning G. B., Hertz B. G. and Broadbent D. E. (1975) Some experiments bearing on the hypothesis that the visual system analyzes spatial patterns in independent bands of spatial frequency. Vision Res. 15, 887-899.

106.5

Jones R. M. and Tulunay-Keesey U. (1975) Local retinal adaptation and spatial frequency channels. Vision Res. 15, 1239-1244. Nachmias J., Sansbury R., Vassilev A. and Weber A. (1973) Adaptation to square-wave gratings: in search of the elusive third harmonic. Yision Res. 13, 1335-1342. Pantle A. (1974) Visual I~ormation Processing of Complex Imagery. Report AMRL-TR-74-43, Aerospace Med. Res. Lab., Aerospace Med. Div., Air Force Systems Command, Wright-Patterson Air Force Base, OH 45433. Pantle A. and Sekuler R. (1968) Size-detecting mechanisms in human vision. Science 162, 1146-l 148. Ratliff F. (1965) Mach Bands: Quantitative Studies on Neural Ne~orks in the Retina. HoIden-Day, San Francisco. Sachs M. B., Nachmias J. and Robson J. G. (1971) Spatialfrequency channels in human vision. J. opt. Sot. Am. 61, 11761186. Stecher S., Sigel C., and Lange R. B. (1973) Composite adaptation and spatial frequency interactions. Vision Res. 13, 2527-2531. Stromeyer C. F. III and Klein S. (1974) Spatial frequency channels in human vision as asymmetric (edge) mechanisms. Vision Res. 14, 1409-1420. Thorell L. G. and Albrecht D. G. (in preparation). Tolhurst D. J. (1972) Adaptation to square-Gave gratings: inhibition between spatial frequency channels in the human visual system. J. Physiol., Lond. 224, 231-248.