Stimulus specificity in the human visual system

Vision

Rcs.Vol.13,pp. 1915-1931. Pergamoa Prrss1973.RIntcdin Grcat Btitsin.

STIMULUS SPECIFICITY IN THE HUMAN VISUAL SYSTEM COLIN BLAKJZMOIXE, JAMES P. J. MUNCEY and ROSALIND M.

RIDLEY’

The Physiological Laboratory, University of Cambridge, Cambridge, CB2 3EG and the Psychological Laboratory, University of Cambridge, Cambridge CB2 3EB (Received 27 March 1973)

A G~T dea1 is known about the coding properties of neurones early in the visual pathway. Each ce11exhibits selettive sensitivity for certain characteristics of the images falliag on its receptive field: it has a trigger feature to which it is specifically tuned. For instante, neurones in the visual cortex of cats and monkeys are selectively sensitive to the orientation and dimensions of bar-shaped patterns of light (HUBEL and WIESEL,1962, 1968). It is generally assumed that orientation- and size-detecting cells like these are involved in the analysis of the shapes of objects. This physiological evidente for the fragmentation of sensory processing has prompted much enquiry into the elements of human visual perception. What are the trigger features of human visual neurones? When a human subject has looked at any powerful visual stimulus he is left with an aftereffeet that depends on the stimulus he has seen. For example, GILINSKY(1968) and BLAKEMORE and CMBW~L (1969a) found that observation of a high-contrast pattern of light and dark stripes (a grating) makes it more difficult, immediately afterwards, to distinguish a low-contrast version of the same pattern. Significantly, test gratings very different in orientation from the high-contrast adapting grating are not made less visible. Such a stimulus-specific aftereffect could be due to the selettive adaptation or desensitization of a particular population of orientation sensitive neurones. This view was reinforced by the discovery that threshold elevation after adapting to a grating is limited to test gratings of similar bar-width or spatial frequency (PANTLE and SEKULER, 1968; BMKENORE and CAMPBELL,1969b). There is an obvious analogy to the fact that cat and monkey cortical cells are selettive for the width of single bars (HUBEL and WXESEL,1962, 1968) and for the spatial frequency of gratings (CAMPBELL,Coopm and ENROT~-C~GELL,1969). The detection threshold is not the only aspect of perception that can be intluenced after adapting to a grating. Indeed, BLAKEMORE and S~rrro~ (1969) suggested that there are at least four classes of aftereffect that might be expected to follow stimulus-specific adaptation: the elevation of threshold for similar stimuli is a Cluss 2 aftereffect. They also argued that test stimuli slightly different from the adapting pattem should appear changed in quality : distortion aftereffects of this kind are called Class 4. For instante, GIBSON(1933) noticed that the apparent orientation of one grating can be changed by adapting to another; BLAKEMORE and SUTTON(1969) and BLAKEMORE, NACHMLUand Svno~ (1970) found that the spatial frequency of test patterns can also appear changed, presumably because of imbalance in the sensitivities of neural channels with somewhat different optimum spatial frequencies. t Present address: Institute of Psychiatry, De Crespigny Park, Denmark Hilf, London S.E.5. 1915

1916

Com

BLAKE..ORE,JA,
MUNCEY hm

ROSALI‘FD M. RIDLEY

Cluss 3 aftereffects are the “opponent” sensations that sometimes arise, for example the apparent spontaneous movement that occurs after adapting to a pattern moving in the opposite direction. Finally, Group Z aftereffects involve a reduction in the apparent strength of the adapting pattern itself and of similar patterns viewed afterwards. A high-contrast grating does indeed seem gradually to fade, and lower-contrast gratings, seen afterwards, appear reduced in contrast (BLAKEMORE, MUNCEYand RIDLEY,1971). Here we describe this phenomenon in more detail and in particular use it to measure the stimulus-selectivity of the human visual system at suprathreshold levels. Definitions

Spatial frequency: Contrast :

number of cycles of a grating per degree of visual angle (c/deg). I tnPI

-

L

+ 4ni”

Imin

where J,,,,, Zminare the maximum and minimum lumi-

nances in a grating. Mean luminance : Ottave :

4nax+ 4ll,n 2

change in spatial frequency by a factor of two.

METHODS The Observer sat at a distante of l-14 m from two oscilloscope screens, both masked down to rectangles 4’ wide and 3” high, arranged one above the other with a gap of 24’ between them. In the middle of this gap was a luminous horizontal fixation bar 30’ long and 4’ in height. CAMPBELLand GREEN’S(1965) simple television technique was used to display vertical gratings, with a sinusoidal luminance profile orthogonal to the stripes, on either or both oscilloscope screens. Each grating could be turned on and off, and the spatial frequency and contra.% varied without appreciably changing the overall mean luminance of the screen, which was about 4.8 cd/m’ throughout. The dim background luminance was about 0.1 cd/m2. The subject held a logarithmic potentiometer that he turned to vary the contrast on the lower screen and he pressed a button to print out the contrast setting. His task was usually to adjust the contrast of the lower grating unti1 it appeared to be the same as that of the upper grating while he fixated the bar between them. Above the two oscilloscopes, at the same distante from the Observer. was a large sheet of translucent opal perspex (Plexiglas) masked down to two transilluminated rectangles, identica1 in size and arrangement to the screens below, with a tixation bar in between. Over the upper rectangular area was a negative of a photograph of a grating of 8.4 c/deg, mounted in a rotatable frame, SOthat it could be set to any orientation. The apertures were transilluminated by two projectors with appropriate filters to make the mean luminance of both the grating and the blank area 4.8 cd/m’, and to match their colours to the yellow-green of the P-31 phosphor of the oscilloscope. The contrast of the transilluminated grating was 0.7.

Part 1. The contrast reduction phenomenon

First we present our experiments on the general properties of this contra& reduction phenomenon. Then in Parts 2 and 3 the aftereffect is used to measure the stimulus specificity of human visual mechanisms. The time-constant of induction. The subject stared at the fixation bar between the two blank oscilloscope screens, and every 10 sec a grating of 5 c/deg appeared on both screens. The subject quickly (in l-2 sec) matched the contrast on the lower screen to that of the test pattern on the upper and both were turned off. After the sixth such baseline setting, the lower grating was extinguished but the upper one was replaced by an adapting grating, also of 5 c/deg, at a contrast of 0.7. Now the subject was adapting his visual field above the

Stimulus Specif-tcity in the Human Visual System

1917

fixation bar to the grating while the part beiow was oniy light-adapted. During adaptation the subject let his gaze drift from side to side across the bar to prevent the formation of a conventional retina1 negative afterimage of the adapting pattern. Every 10 sec, during adaptation, the same origina1 test grating appeared above, with a comparison pattem below, and the subject matched the contrasts. The adapting display reappeared for a further 10 sec before the next setting. After twenty such judgements, interposed within the period of adaptation, the upper pattern also disappeared between Baseline, 0

Recovery,

Sec 50

0

0

50

100

150

50

100

sec 150

200

Adaptatian FIG. 1. Every 10 sec a test grating of 5 c/deg appeared on the upper screen and a comparison grating, also 5 c/deg, on the lower screen. The subject adjusted the contrast of the comparison grating to match that of the test grating, while fìxating between them. During the “baseline” and “recovery” periods both screens went blank between settings, but in the “adaptation” period the upper test grating was replaced by a 5 c/deg grating at a contrast of O-7. Three different contrasts of test gratings were used: 0.7 (rectangles and squares), 056 (triangies) and 0.32 (circles). (a) The contrast setting on the lower screen (i.e. the apparent contrast of the upper test grating) appears on the ordinate. The actual contrasts of the test gratings are marked by filled arrowheads. Each point is the mean of N = 4. The rectangles, used to plot the data for test gratings of 0.7 contrast, have a height of twice the S.E. (b) The same data are normalized on the ordinate where zero is the true contrast of the test gratmg.

readings in order to foliow the time-course of recovery. This whole procedure was carried out four times for every particular test condition, aliowing at least 30 min between each session and the next, for full recovery. The solid rectangles in Fig. l(a) show the results for test gratings of the same contrast, O-7, as that of the adapting pattern, SO these symbols follow the change in apparent contrast for the adapting grating itself. The ordinate is the contrast on the lower screen and each.rectangle has a height of twice the SE. of the settings (1%’= 4, as in almost al1 the experiments). The average S.E. was in fact only about 0.02 log units. Clearly the subject was able to match the contrast with considerable accuracy before

1918

COLIS BLAKEMORE,

JAMES P. J. MUNCEY ANDR~Y,ALISD IM.RIDLEY

adapting; the apparent contrast of the upper grating fell during adaptation, with a timeconstant of about 30 sec, and rose gradually afterwards. For the triangles in Fig l(a) the test grating had a contrast of O-56 and for the circles it was O-32. It is evident that the magnitude of the reduction in apparent contrast increased as the test grating was made lower in contrast. This is particularly clear in Fig. l(b) where the results are normalized at the true test contrast on the ordinate, which now indicates the reduction in apparent contrast for test gratings of 0.7 (squares), 0.56 (triangles) and 0.32 contrast (circles). This whole experiment was repeated with another subject (JM) at 5 c/deg and with both subjects at a different spatial frequency, 10 c/deg. The general time-course and magnitudes of the changes in apparent contrast were very similar. The time-course ofrecovery. It is clear that both the increase in contrast threshold (BLAKEMOREand CA~BELL, 1969b) and the perceived spatial frequency shift (BLAKEMORE et al., 1970), which follow adaptation to a gratin g, depend for their magnitude and their timecourse on the length of time spent in adaptation. We tested whether this is true of contrast reduction in the following way. The experiment of Fig. l(a) was repeated using a 5 c/deg, 0.7 contrast adapting grating and a 5 c/deg, 0.18 contrast, test grating. The subject, CB, made only two baseline, unadapted settings, 5 sec apart, and then adapted without interruption to the high-contrast grating on the upper screen. Immediately after adaptation the test grating appeared on the upper screen with a comparison pattern below and the subject made a match. These patterns were removed and reappeared 5 sec later for a further match, and SOon unti1 recovery was complete. Figure 2 shows the results of varying the length of time for adaptation, from 5 sec to 5 min. Each point is only a single observation but it is still quite obvious that: (1) The initial magnitude of the contrast reduction increases up to a maximum of about 0.8 log units, after about 45 sec of adaptation, and does not increase further for longer adapting times. (2) The time-constant of recovery continues to lengthen, SOthat it takes about 6 min to recover completely from 5 min exposure. These properties of this phenomenon are very similar to those of the other aftereffects of adapting to a grating. SimpliJicationof the method of measurement. At this point we were in a position to change the procedure and measure only the maximum contrast reduction, immediately after adaptation, knowing that an adapting period of more than about 1 min maximized the effect. Four initial, unadapted baseline settings were taken 10 sec apart (for each different contrast of the test grating), then the subject adapted for 2 min, after which the adapting grating was replaced by the first test grating: he made a contrast match, and then continued to adapt for a further 10 sec before the next test match. Four such readings for each different test contrast were taken; this procedure of “topping-up” the adaptation kept the settings quite consistent. SO for each adapting and test condition in al1 the following experiments we were able to subtract the mean contrast setting during adaptation from that during the preceding baseline matches, in order to assess the reduction in apparent contrast. The e#ect of the contrast of the test pattern. Figure 3 shows the results of adapting to a gratin; of 5 c/deg, O-7 contrast, and testing with different contrast levels, also at 5 c/deg. The open arrowhead points to the original, unadapted contrast threshold (on the abscissa) while the solid arrowhead is the elevated threshold, after adaptation, for subject CB (means of N = 4). The solid square then plots (on the ordinate) the increase in threshold contrast

Stimuius Specifcity in the Human Visual System

1919

(i.e. the horizontai separation of open and solid arrows), whiie the open and solid circles

show the apparent contrast reduction at different test contrasts. Thìs graph illustrates the way that the magnitude of the effect increases with decreasing test contra& and the fact that threshold elevation is apparently just a special case of contrast reductìon. E Recovery,

sec

0.18

0.

Ia

0.18 04 8

0.18

0.16

0.18 0.18

min

048

-4

’

1

1 2

I

l

3

4

I 5

I 6

1 7

Recovery, min FIG. 2. In this experiment the test grating on the upper screen always had a contrast of 0.18 and the adapting grating, which replaced it during the period marked “adaptation” was at a contrast of 0.7. Bach point is a singk setting of thecontrast of a comparison gratins on the lower screen, which appeared at the same time as the upper test grating and was used to measure the apparent contrast of the latter. There are two settings before adaptation and several, taken every 5 or 10 sec, after adaptation. Each CUIW is displaced on the ordinate and in each case the starting poiat is shown by the actuaì contrast of the test grating. O-18. The decline in apparent contrast is indicated by the inset vertical scale. At the end of each set of points is the length of time spent in adaptation. (Subject CB. Spatial frequeacy 5 c/deg.)

Part 2. The orientation specijikity of contrast reductiun

In order to determine whether contrast reduction depends on the relative orientation of the adapting and test gratings, the rotatable, transilluminated grating mounted above the oscilloscope was used for adaptation. The subject fìxated the bar between the rotatable grating (8.4 c/deg, 0.7 contrast) and the blank rectangular aperture below. Thus the retina1 stimulation was identica1 to that during adaptation in Par-t 1, except that the orientation of the adapting pattern could be changed. After the norma1 2 min of adaptation the subject glanced down at the fìxation bar between the two oscilloscopes, on which were vertical

COLIS BLAKEMORE,JAMESP. J. MUNCEY A‘~D ROSALJSD M. RIDLEY

1920

u)

cE

-1.0

vo-

z

n

zf

o 0

0

è .E t

:

2

-

O

$2 OS-

0

c 0 ” c ,m 0

2

Q

0.5

l

% L

l

0

0.01

0

w

-G

I

I

I

1 I IlllI 0.05

Contrast

l

grating,

l

I lIIl_ 0.5

0.1 of test

l

log

l.0”

units

FIG. 3. Each circle, filled for CB, open for JM, is the reduction in apparent contrast for a test grating (5 c/deg) appearing immediately after an adapting grating (5 c/deg; 0.7 contrast). Different contrasts of test grating were used, as indicatedon the abscissa.The open arrowhead points to the threshold contrast of a 5 c/deg grating before adaptation, while the filled arrow-

head shows the increased threshold after adapting to a 0.7 contrast grating (Subject CB). The horizontal separation of the two arrowheads (the elevation of threshold) is plotted on the ordinate as a filled square above the filled arrowhead. Each point is the mean of .V = 4.

test and comparison patterns (also of 8.4 c/deg) which he matched in contrast. He looked back at the adapting array for 10 sec between successive readings. Figure 4 shows the results of adapting to many different orientations (45’ anticlockwise from the vertical to 40” clockwise) and testing with many different conttasts (from 0.7 down to 0.6) for an 8.4 c/deg vertical grating. In each case the apparent contrast is reduced most after adapting to a vertical grating (zero on the abscissa) and there is no significant effect after adapting to a grating rotated 45” to the vertical. Obviously this aftereffect is orientation specific. The equivalent contrast transformation. Since the overall magnitude of the apparent contrast reduction varies with the contrast of the test grating it is impossible to make a simple direct comparison of the orientation specificity for different test contrasts. TO try to circumvent this problem we used a strategy introduced by BLAKEMOF~E and NACHMLG (197 1) for the comparison of aftereffects. The technique involves the measurement of the decline of the aftereffect with the reduction in contrast of a correctly-orientated adapting grating. Once this function is known it is then possible to describe the diminution in the effect as the adapting grating is tilted as zy it were a reduction in the contrast of an appropriately orientated adapting grating. This can be done for each test contra& thus reducing each function to a description of the equivale& contrast of a vertical adapting grating for a change in orientation of the lixed-contrast adapting grating. First it was necessary to measure the influente of the contrast of a vertical adapting

grating, and this was done with the two oscilloscopes. The adapting pattern on the upper screen was set to 8.4 c/deg and its contra9 was varied (from O-13 to O-7) for different sessions. For each different adapting contrast we measured the reduction in apparent contrast for many different contrasts of the test grating (which was also 8.4 c/deg). In each case the magnitude of the contrast reduction decreased as the adapting pattern was reduced in contrast, and some of the results are plotted on the right in Fig. 5. This shows the reduction in apparent contrast for four different test contra& (0.7, 0.35, O-18

Stimulus Specifìcity in the Human Visual System eo ‘F.

1.0

1921

Vertical 0 o 0.7 ‘0 0 050 ~00.35 Orno.25 6 A 0.18 0 AO.13 (l v 0.09

4 vo06 -----------

2

Contrast threshold 0.02 50

I 40

I 30

I 20

l IO

l IO

0

Anticlockwise

l 20

I 30

I 40

Clockwise

Orientation

of adapting

groting,

deg

FIG. 4. The points plot the apparent contrast of vertical test gratings, of 8.4 c/deg, immediately after adapting to gratings, also of 8.4 c/deg, al1 at a contrast of 0.7, but at different orientations. The open arrows on the right indicate the average setting of apparent contrast before adaptation. for the test contrast whose symbol is shown near the arrow. Next to each symbol is the actual contrast of the test grating. The interrupted line is the contrast threshold at 8.4 c/deg: no points appear below this line because a grating with an apparent contrast less than this value is invisible and cannot be matched in contrast. (Subject CB, N = 4.) Test

contrast 0.7

-10.75 0

0.75r

Orientotion

of adapting

grating,

deg

Contrastof

vertical

adapting

grating

FIG. 5. Some of the data from Fig. 4 are reproduced on the left, using the same symbols. Four different test contrast are illustrated. Each point plots the reduction in apparent contrast, i.e. the difierence between the matched contrast during adaptation and the match made before adaptation (shown by the open arrows in Fig. 4). For the data on the right the subject adapted to vertical test gratings of difTerent contra& and measured the reduction in apparent contrast for vertical test gratings of the same four contrast levels (0.7,0*35,0-18 and 0.13). Regression lines are fitted to the points by the method of least squares. (Subject CB, N = 4. Spati1 frequency = 8.4 c/deg throughout.)

1922

COLIN BLAKEMORE,JA.WS P. J. MUWEY A~P ROSALIXDM. RIDLEY

and O-13)as a function of the contrast of the vertical adapting grating. Fortunately, on these logarithmic co-ordinates, the points are quite well fitted by straight lines and the method of least squares was used to draw a regression line through each set of data. (The average coefficient of correlation is about 0.97.) On the left side of Fig. 5 are some of the data from Fig. 4 plotted as the reduction in apparent contrast as a function of the orientation of the adapting pattern (pooling clockwise and anticlockwise data). The four test contrasts illustrated are exactly the same as those chosen for the right hand set of curves and the ordinates are exactly aligned. Again regression lines are fitted through the points and the fit is very good (average coefficient of correlation = O-97).

(b)

w

Oriantotion

of adopting

groting,

deg

FIG.6(a). These curves are transformed from the data of Fig. 5 as described in the text. Each line plots, for the vertical test grating whose constant is shown next to the line, the contrast of a vertical adapting grating that produces the same amount of apparent contrast reduction as a 0.7 contrast grating, whose orientation appears on the abscissa. The filled arrowhead marks an equivalent contrast of 0.7 and aU the lines should lie near this value at zero on the abscissa (vertical adapting grating). (Subject CB. Spatial frequency 8.4 c/deg.) (b) Data transformed in exactly the same way for subject JM. The test contrasts analysed were 0.5, 0.X and 0.09. (Spatial frequency, 8.4 c/deg.)

Now the equivalent contrast transformation can be performed using these fitted straight lines. For any particular test contrast a change in orientation of the 0.7 contrast adapting grating can be expressed as if it were a change in contrast of a vertical adapting grating. Figure 6(a) shows the result of this transformation for the four test contrasts. The ordinate is now the equivalent contrast of a vertical grating, while the abscissa is the actual orientation of a 0.7 contrast adapting grating. Since the co-ordinates are the same as in Fig. 5 the functions must be straight lines, and they should cross the ordinate close to 0.7, the actual contrast of the rotatable grating. Al1 four Iines do SO, and what is more they have roughly the same slope. The functions are in fact exponential and the half width at half amplitude is about 8”, much the same as BLAKEMORE and NACHMIAS (1971) found for this same subject (CB), for both threshold elevation and the perceived spatial frequency shift. What is most important is that the orientation specificity, measured in this way, is virtually identica1 whatever the contrast of the test grating.

Stimulus Spcifìcity

in the Human Visual System

1923

Figure 6(b) shows the fina1 result of the same transformation for subject JM, but for three other test contrasts (0.50-25 and 0.09). Again the three functions are similar and are themselves of much the same slope as those for CB. Part 3. The spatial frequency specifcity of contrast reduction The intention in these experiments was similar in logic to the preceding section. We wanted to determine whether the aftereffect is specific for the spatial frequency of the test grating by adapting to vertical gratings of many different spatial frequencies and measuring the contrast reduction for one particular spatial frequency. However, first the contrasts of the adapting gratings had to be equated in some way to make them al1 equally “effettive” as adapting stimuli, because the contrast sensitivity of the visual system varies SOdramatically with the frequency of a grating. There are at least three possible criteria for equating the contrasts of adapting patterns of different spatial frequency : (1) The gratings could be made identica1 in absolute, physical contrast; (2) The gratings could be set at some arbitrary number of units (linear or logarithmic) above contrast threshold at each frequency; (3) The gratings could be made equa1 in their apparent contrasts, SOthat al1 the adapting patterns seemed to be very similar in contrast. We thought it best to use this last criterion, assuming that gratings that appear equa1 in contrast would be having similar excitatory effects on the visual system. SO first the apparent iso-contrast functions were determined for different spatial frequencies, in a similar way to that of BRYNGDAHL (1966) and of WATANABE,MORI, NAGATAand HIWATASHI (1968). Apparent iso-contrast functions. The subject looked at the bar between the two screens and the grating above was set to 5 c/deg throughout. The grating below was varied in spatial frequency and the subject’s task was to adjust its contrast unti1 it seemed to be the same as that above, even when they were different in spatial frequency. The two observers found this odd task quite easy and the variance of the judgements was hardly any larger than that when the gratings were identica1 in frequency. Figure 7 shows the results for both subjects for three different fixed contrast levels of the upper standard grating: O-7 (circles), 0.22 (squares) and 0.07 (upright triangles). The inverted triangles and interrupted lines plot the familiar contrast-threshold function determined by asking the subject to set the contrast of gratings of different spatial frequency on the lower screen unti1 he could only just resolve them, while the upper screen was blank. For both subjects we found, as did BRYNGDAHL (1966) and WATANABE et al. (1968), that the apparent iso-contrast functions became flatter at higher contrasts. Indeed the standard grating of O-7 contrast was matched with gratings of just about the same physical contrast, whatever their frequency, within the range we explored. Therefore in our experiment the subject simply adapted to gratings of different frequency, al1 at O-7 contrast, thus satisfying criterion (3) [and, incidentally, criterion (1)] for the equation of adapting patterns. Spatial frequency sensitivity at 84 cldeg. The subject adapted to vertical patterns on the upper oscilloscope, as in Part 1, but the spatial frequency was varied from 2.1 to 23.8 c/deg while the test gratings were always fìxed at 8.4 c/deg. For the lower spatial frequencies (5 c/deg and below) the adapting pattern was shifted slowly from side to side, with an amplitude of about 1.5 cycles of the pattern, about 0.5 times/sec, by injecting an extra

1924

Corrii

BLAKEMORE, JAMES P. J. MUNCEY ASD ROSALI~D M. RIDLEY

triangular Signa1into the timebase amplifier of the oscilloscope. This avoided the formation of a negative afterimage of the grating. Figure 8 shows results in a similar fashion to those in Fig. 4, but now the abscissa is the spatial frequency of the adapting pattern generated on the upper screen (contrast 0.7 throughout) and the ordinate is the apparent contrast of test gratings, always of 8-4 c/deg.

rl Spgtial

I

2 frequency

Il

IIIIII 5

l IO

of lower grating,

20 c/deg

FIG. 7. Lines of apparent iso-contrast. The subject fixated between two gratings, the spatial frequency of the upper one being 5 c/deg throughout. The spatial Frequency of the lower grating was varied, as shown on the abscissa, and its contrast was adjusted unti1 it seemed similar to the 5 cjdeg standard grating above. There were three different contrasts For this standard grating, marked by open arrowheads: 0.7 (circles), 0.22 (squares) and 0.07 (upright triangles). The large symbols plotted at 5 c/deg on the abscissa show the results when upper and lower gratings were identica1 in spatial Frequency. The inverted triangles and interrupted lines show the threshold contrast function determined by setting the contrast of the lower grating unti1 it was just visible, For different spatial Frequencies. (Subject CB, filled symbols. Subject JM, open symbols.)

The family of curves shows the data for many different test contrasts. It is evident that the aftereffect is specific for spatial frequency and that the maximum effect is caused by adapting to a grating that is also 8.4 c/deg. On this logarithmic abscissa, the effect declines more slowly as the adapting frequency is made lower than that of the test grating, and falls quickly as it is made higher. In general, adapting gratings more than about 2 octaves away in frequency have almost no influente. The equivalent contrast transformation. In Fig. 9 the same transformation as in Fig. 5 is performed but now the data on the left are those for different adapting frequencies. The

Stimuius

Specificity

in the Human Visuai System

E

lJ

1925

0 0.7

0 00.5

0.5 -

0

cl 0.35

(l

n 0.25

0

LI 0.18

0

A 0.13

0

v 0.09

0

70.06

0.2 -

0.1 -

0~0~ -

t

Contrast

threshold

_____-__-_-.---_------

QOZ-

I 2 Spatial

I

i

t Irrlrl

10 5 frequency of adopting

20 grating,

I c/deg

FIG. 8. Results of an experiment simi& to that for Fig. 4, except that the spatial frequency of the adapting grating was varied. fts contrast was always O-7. The spatial frequency of the test grating was always 8.4 c/deg but its contrast was varied from 0.7 to O-06 as indicated by the baseline unadapted settings on the right. (Subject CB, N = 4, Orientation vertical throughout.)

SpaTial 2

f requency, I

0

octaves I

2 0.25 0

P .s

0.25 $ I E t 0.5 4 L

5

0.25 u; I $ 0 075 o c 0.5 z Ei Q a 0.25 0 Spotial

frequency grating,

of adopting c/deg

Conhast

of 8~4cldeg adaptiW grating

9. A set of graphs, like those in Fig. 5, except that the data on the left, calculated from Fig. 8, show the apparent contrast reduction for 8.4 cfdeg test gratin8s after adapting to O-7 contrast gratings of different spatial frequencies. The upper abscissa on the teft shows the spatiai frequency of the adapting grating in octaves on each side of 8.4 c/deg. The same four contrasts of the test gratings are analysed as in Fig. 5. and the data on the right are identical. (Subject CB, lV = 4. Orientation verti& throughout.) FIG.

1926

CON BLAKEMORE, JW

P. J. MUNCEYASD

ROSALBD

M. RIDLEY

results are illustrated for the same four test contrasts used for Fig. 5, and the right hand portion of Fig. 9 is therefore identica1 to that of Fig. 5. Since the functions in Fig. 8 are not symmetrical about 8.4 c/deg, data could not be pooled for adapting frequencies on the two sides of the peak. Therefore they are reproduced completely, and again the decline in the aftereffect wrth changing adapting frequency in both low and high frequency directions is always well fitted by a straight regression line (average coefficient of correlation = O-98). SO, in Fig. 10, the equivalent contrast transformations are sets of straight lines whose peaks should al1 be close to 0.7 on the ordinate. Once again the four transformed curves are frequency,

Spatial

octaves

r i

2 Spatial

I

I

,

I

(II

4

frequency of adapting

IO grating,

20

30

c/deg

FIG. 10. The equivalentcontrast transformation for the data of Fig. 9. Each curve shows the contrast of an 8.4 c/deg adapting grating that produces the same magnitude of apparent contrast reduction as a 0.7 contrast grating of the spatial frequency shown on the abscissa. The spatial frequency of the test grating was always 8.4 c/deg and four different test contrasts, indicated next to the curves, are analysed. (Subject CB. Orientation vertical throughout.)

very similar to each other, showing that the frequency specificity of the aftereffect is much the same for al1 test contrasts. The full width at half amplitude is in fact about O-75 octaves and the decline of equivalent contrast is approximately a power law on both sides of the peak. Spatial frequency sensitivirj at 5 cldeg. The whole experiment was repeated for both subjects with test gratings of 5 c/deg. First the Observer adapted at many different spatial frequencies and tested the aftereffect at many different contrasts for test gratings of 5 c/deg. Then he adapted to many different contrasts of the 5 c/deg adapting grating and again tested the strength of the aftereffect. SO we were able to perform the equivalent contrast transformation as in Fig. 9, although the regression lines were not quite such good fits as for the data for 8-4 c/deg (average coefficient of correlation = 0.94).

Stimuius Specikity

Spatial

w

2

3

10

Spatial

1927

in the Human Visual System

frequency,

20

t

otives

2

c

5

frequency of adcpting qrating,

10

2u

c/deg

FIG. 11. Results of identica1 experiments to those described by Figs. 8-10, but the test grating always had a spatial frequency of 5 c/deg. Also, in the experiment in which the contrast of the adapting grating was varied (as in the right hand curves of Fig. 9) the spatial frequency of the adapting pattetn was also 5 c/deg. (a) Subject CB. Four different test contrasts are analysed, as shown next to the functions. (b) Subject JM. Three other test contrasts are analysed.

The fina1 results are shown as equivalent contrast transformations far the two subjects in Fig. Il. The test contrasts used in the analysis were just the same as for Fig. 6. The sets of functions are al1 very similar to each other and basically much the same in bandwidth as those of Fig. 10. DISCUSSION

Not only does adapting to a grating increase an observer’s contrast threshold for similar patterns, but it also decreases the apparent contrast of suprathreshold gratings. This appare& contrusr reduction is similar in its time-course for induction (Fig. 1) and recovery (Figs. 1 and 2) to the threshold elevation phenomenon (BLAKJXW and CAMPBELL, 1969b). Indeed it seems reasonable to consider the change in threshold itself as merely a special case of apparent contrast reduction. After adapting to a very high-contrast grating, lowcontrast test gratings are more strongly influenced than high-contrast ones (Fig. 3). This phenomenon gave us an opportunity to measure the orientation-selectivity and spatial frequency-selectivity of the human visual system at suprathreshold levels of contrast, beyond the traditional confìnes of psy~ho-physical thresholds. In norma1 photopic conditions our visual systems are analysing the shapes and motion of suprathreshold patterns. Surely it is more important to know the coding properties of the visual system at norma1 working contrasts than near the threshold level. In fact adapting to a high-contrast grating alters the apparent contrast only for test gratings of similar orientation (Fig. 4) and spatiai frequency (Fig. S), and over roughly similar ranges to those over which the threshold is raised. In order to compare quantitatively the tuning characteristics of apparent contrast reduction for different test contrasts we employed the equivalent contrast transformation, described by BLAKEMOREand NACHMIAS

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P. J. IMUNCEY AND ROSALIND 1U.RIDLEY

(1971). TO do this the apparent contrast reduction was also measured after adapting to gratings of various contrasts, but always of the same orientation and spatial frequency as the test gratings [Fig. 5(b)]. Then we were able to describe the declining aftereffect with increasing discrepancy between adapting and test orientations just as if the orientation of the adapting grating were the same as that of the test, but its contrast was reduced (Fig. 5). When this is done the tuning characteristics turn out to be almost identical, whatever the test contrast (Fig. 6)-and very much the same as those defined by threshold elevation (BLAKEMORE and NACH;WAS,1971; MOVSHONand BLAKEMORE in preparation). The decline of the aftereffect varies exponentially with relative orientation and the half-width of the function is of the order of 8”. Exactly the same equivalent contrast transformation can be applied to describe the spatial frequency selectivity of the aftereffect (Fig. 9). Now a change in the spatial frequency of the adapting grating can be represented as if it were a reduction in adapting contrast (Figs. 10 and 11). Again this procedure resolves the differences in tuning for different test contrasts and shows that for both subjects, with test gratings of 8.4 and 5 c/deg, the spatial selectivities are quite similar. This al1 confirms the power of the equivalent contrast transformation in reducing the data from experiments such as these, and in describing the stimulus specificities of visual aftereffects. The tuning characteristics for spatial frequency are quite clearly not symmetrical about the test frequency on a logarithmic abscissa plot (Figs. 10 and 11). The aftereffect declines rapidly as the adapting grating is increased in spatial frequency compared with the test grating, and it falls more slowly as the adapting spatial frequency is reduced. This asymmetry presumably reflects the sharper high spatial frequency attenuation exhibited by neurones in the visual pathway when responding to gratings (ENROTH-CUGELL and ROBSON, 1966; CAMPBELLet al., 1969; CAMPBELL,COOPER,ROBSONand SACHS,1969). BLAKE~IORE and CAMPBELL(1969b) reported a similar asymmetric tuning for the threshold elevation phenomenon, but in their case the adapting grating was fixed in spatial frequency and the test spatial frequency was varied. This should of course be expected to produce an asymmetry that mirrors the tuning characteristics of the neurones involved, unlike our procedure in which we tested at one frequency and adapted at many. Perhaps this apparent discrepancy is explained by the rapid decline of absolute contrast sensitivity with increasing spatial frequency that characterizes the overall sensitivity function for the visual system above about 3 c/deg. Presumably neurones with very high optimal spatial frequencies have much lower absolute contrast sensitivity at their best spatial frequency than do cells tuned to lower spatial frequencies. In this case the tuning characteristics discovered by adapting at one spatial frequency and testing at many are not simply related to the sensitivity functions for the individua1 neurones concerned. The spatial-frequency selectivity of the channels exposed by contrast reduction is very similar in bandwidth to that revealed by the threshold elevation phenomenon (BLAKEMORE and CAMPBELL,1969b). They are also virtually identica1 to the tuning characteristics found by STROMEYER and JULESZ(1972), who used filtered one-dimensiona1 visual noise to mask test gratings. This latter technique also measures spatial frequency sensitivity at high test contrasts, above the absolute contrast threshold, SO it is gratifying to set such good agreement. There remains the problem that spatial filters with characteristics as broad as these seem inappropriate for the sort of Fourier analysis of the visual image proposed by CAMPBELL and ROBSON(1968), BLAKEMORE and CAMPBELL(1969b) and many others. There is a marked

Stimulus Specitìcity in the Human Visual System

1929

disagreement with the results of experiments involving the detection threshold for complex gratings consisting of two similar spatial frequencies mixed together (SACHS, NACHMIAS and ROELSON, 1971). Those experiments led to the conclusion that the bandwidth of spatial filters can be extremely narrow. There is a possible resolution to these conflicting results. It could well be, as TOLHURST(1972) suggests, that spatial frequency channels inhibit each other, in order to improve their tuning characteristics: BLAKEMORE,CAWENTERand GEORGESON (1970) and CARPENTER and BLAKEMORE (1973) have proposed the same mutua1 inhibition between human orientation selettive mechanisms. If this is the case then aftereffects of adaptation may be due to prolonged inhibition rather than to over-excitation (BLAKEMORE, CARPENTER and GEORGESON, 1971). In that case, adaptation experiments (and those involving simultaneous masking) may be measuring the broad tuning properties of this inhibition, rather than the excitatory tuning characteristics themselves. Incidentally, the monotonie relationships between contrast reduction and adapting contrast for al1 test contrasts [Fig. 5(b)] imply that this aftereffect is not specifically tied to the adapting contrast itself. If the neural mechanisms involved in apparent contrast reduction were seiectively sensitive to the contrast of gratings, we might expect each adapting pattem only to influente test gratings of similar contrast. Since this is not the case, we conclude that the neurones involved in this perceptual phenomenon are not specifically tuned to certain contrast levels but that they increase their responses monotonically with increasing contrast. Now a detailed pitture emerges of the perceptual consequences of adapting to a highcontrast grating, which presumably selectively desensitizes a particular population of featuredetecting neurones. First, the detection threshold is raised for similar pattems (GILINSKY, 1968; BLAKEMOREand CAMPBELL, 1969b; PANTLEand SEKULER,1968). Second, test gratings of somewhat different angle appear to be changed in orientation (GIBSON, 1933), while those of different spatial frequency seem to change their frequency (BLAKEMORE et al., 1970). Finally, similar suprathreshold test gratings seem reduced in apparent contrast. Al1 this adds up to a substantial case in favour of the hypothesis that the human visual system containes neurones that are selectively sensitive to the orientation and dimensions of retina1 images. Acknowle&ements-We are grateful to the Medica1 Research Council, London, for suppot-ting this research (Grants No. G970/807/B and No. G972/463/B).

REFERENCES BLAKEMORE,C. and CAMPBELL,F. W. (1969a). Adaptation to spatial stimuli. J. Physiol., Lond. 200,l l-13P. BLAKEMORE,C. and CAMPBELL,F. W. (1969b). On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retina1 images. J. Physiol., Lord. 203,237-260. BLAKEMORE,C. and NACHMIAS,J. (1971). The orientation speciticity of two visual aftereffects. J. Physiol., Lond. 213, 157-174. BLAKEMORE,C. and Srrrro~, P. (1969). Size adaptation; a new aftemffect. Science, N. Y. 166,245-247. BLAKEMORE, C., CARPENTER,R. H. S. and GEORGESON,M. A. (1970). Latera1 inhibition between orientation detectors in the human visual system. Nature, Loti. 228, 37-39. BLAKEMORE. C., CARPENTER,R. H. S. and GEORGESON, M. A. (1971). Latera1 thinkingabout lateral inhibition. Nature, Lond. 234,418-419. BLAKEMORE, C., MUNCEY,J. P. J. and RDLEY. R. M. (1971). Perceptual fading of a stabilized cortical image. Nature, Lond. 233,204-205. BLAKEMORE,C., NACHMIAS,J. and SWITON,P. (1970). The perceived spatial frequency shift: evidente for frequency-selettive neurones in the human brain. J. Physiol., Lord. 210,727-750. BRYNGDAHL,0. (1966). Characteristics of the visual system: psychophysical measurements of the response to spatial sine-wave stimmi in the photopic region. J. opt. Soc. Am. 56, 811-821. V.R.13/10-I

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CAMPBELL,F. W. and GREEN, D. G. (1965). Optical and retina1 factors affecting visual resolution. J. Physiol., Lond. 181, 576593.

C~PBELL, F. W. and ROB~ON,J. G. (1968). Application

of Fourier analysis to the visibility of gratings.

J. Physiol., Lond. 197, 551-566.

CAMPBELL,F. W., COOPER,G. F. and ENROTH-CUGELL,C. (1969). The spatial selectivity of the visual cells of the cat. J. Physiol., Lond. 203, 223-235. CAMPBELL,F. W., C~OPER, G. F., ROB~ON,J. G. and SACHS,M. B. (1969). The spatial selectivity of visual cells of the cat and the squirrel monkey. J. Physiof. Lond. 204, 120-121P. CARPENTER,R. H. S. and BLAKEMORE, C. (1973). Interactions between orientations in human vision. Expl. Brain Res. (in Press). ENROTH-CUGELL,C. and ROBSON,J. G. (1966). The contrast sensitivity of retina1 ganglion cells of the cat. J. Physiol., Lond. 187, 517-552. Gr~t.so~, J. J. (1933). Adaptation, aftereffect and contrast in the perception of curved lines. J. exp. Psychol. 16, 1-31. GILINSKY,A. S. (1968). Orientation-specific effects of patterns of adapting light on visual acuity. J. opc. Soc. Am. 58, 13-18.

HUBEL, D. H. and WIESEL,T. N. (1962). Receptive fields, binocular interaction and functional architetture in the cat’s visual cortex. J. Physiol., Lond. 160, 106-154. HUBEL, D. H. and WIESEL, T. N. (1968). Receptive fields and functional architetture of monkey striate cortex. J. PhysioL 195, 215-243. PAN~LE,A. and SEKULER,R. (1968). Size-detecting mechanisms in human vision. Science, .V. Y. 162, 11461148. SACHS, M. B., NACHMIAS,J. and ROE~ON,J. G. (1971). Spatial-frequency channels in human vision. J. opt. Soc. Am. 61, 1176-1186. STROYMEYER, C. F. 111and JULESZ,B. (1972). Spatial frequency masking in vision: critica1 bands and spread of masking. J. opt. Soc. Am. 62, 1221-1232. TOLHURST,D. J. (1972). Adaptation to square-wave gratings: inhibition between spatial frequency channels in the human visual system. J. Physiok, Lond. 226, 231-248. WATANABE,A., MORI, T., NAGATA,S. and HIWATASHI,K. (1968). Spatial sine-wave responses of the human visual system. Vision Res. 8, 1245-1263.

Abstract-During adaptation to a high contrast grating it gradually seems to fade. A lowercontrast test grating appearing directly after the adapting pattern appears reduced in apparent contrast. The orientation specificity and spatial frequency speciflcity of this upparent contrast reduction have been determined by adapting to gratings of various orientations and spatial frequencies. and measuring the contrast reduction for test gratings of fixed orientation and frequency. The sensitivity characteristic for orientation has a half-width at half amplitude of 8’: that for spatial frequency has a full-width at half amplitude of 0.75 octaves. This result is compared with the properties of neurones in the cat and monkey visual cortex.

Résumé-Un réseau à grand centraste semble s’évanouir graduellement par adaptation. Un réseau test à centraste faible apparaissant directement après le réseau d’adaptation semble réduit en centraste. On détermine la spécificité B l’orientation et à la fréquence spatiale de tette réduction du centraste apparent par adaptation à des réseaux d’orientations et fréquences spatiales diverses, en mesurant la réduction de centraste de réseaux tests d’orientation et fréquence frxes. La caractéristique de sensibilité B l’orientation a une demi-largeur pour I’amplitude moitié à S’, celle de la fréquence spatiale a une largeur totale pour l’amplitude moitié &0,75 ottave. On compare ce résultat aux propriétés des neurones dans le cortex visuel du chat et du singe.

Zusamrnenfassung-Wahrend der Adaptation auf ein Gitter mit hohem Kontrast scheint dieses Gitter allmahlich zu venchwinden. Bei niedrigerem Kontrast erscheint das Gitter unmittelbar nach der Adaptationsphase im Kontrast gemindert. Die Parameter dieser Kontrastminderung (Lageabhangigkeit, Ortsfrequenz) wurden untersucht, wobei auf Gitter unterschiedlicher Lagen- und Ortsfrequenzen adaptiert wurde. Dabei wurde die Kontrastminderung fir Gitter vorgegebener Lage und Ortsfrequenz gemessen. Die Kontrastminderung si& auf die Hàlfte b-ei um 8” verdrehten Gittem bzw. bei um 0,75 Oktaven venchobener Ortsfrequenz.Die Messungen werden mit Ergebnissen aus Katzenneuronen und dem visuellen Cortex von Affenverglichen.

Stimulus Specificity in the Human Visual System

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