The effects of V4 lesions on the visual abilities of macaques: hue discrimination and colour constancy

Behavioural Brahz Research, 53 (1993) 51-62 9 1993 Elsevier Science Publishers B.V. All rights rese~'ed. 0166-4328/93/S06.00

51

BBR 01395

The effects of V4 lesions on the visual abilities of macaques: hue discrimination and colour constancy V. W a l s h , D . C a r d e n , S . R . B u t l e r a n d J . J . K u l i k o w s k i Visual Sciences Laboratory. UMIST. Manchester (UK) (Received 15 May 1992) (Revised version received 30 October 1992) (Accepted 2 November 1992)

Key words: Color constancy; Visual cortex; Attention; I lue discrimination; Categorization; Macaque

Monkeys with lesions of cortical visual area V4 were compared with unoperated monkeys in three experiments. In Expt. 1 they were tested for the reacquisition of a pre-opcrativcly learned hue discrimination task. In Expt. 2, as a test of colour constancy, the monkeys were required to perform previously overlearned colour discrimination tasks when the amounts of red, green and blue light in the illuminant were changed. In Expt. 3 the animals were compared on the post-operative acquisition ofhue, greyness and saturation discrimination tasks. The results of Expt. 1 showed that monkeys with V4 lesions can regain their pre-operative levels of performance on hue discrimination tasks. Expt. 2 showed that monkeys with V4 lesions have a colour constancy deficit. Expt. 3 reinforced the finding that the animals with V4 lesions could learn to perform fine hue discriminations but that their final, asymptotic performance was not as reliable as that of normal animals. The wavelength discrimination data are discussed within the context of recent electrophysiological findings that V4 is involved in selective attention to visual stimuli and the constancy data are interpreted as evidence that V4 is important for defining colour constancy thresholds but not for constructing the perceptual categories underlying constant colour perception.

INTRODUCTION

Cortical vist, al area V4 in the macaque monkey has been reported to contain a high concentration of cells which are selective for chromatic information. This is in contrast with other extrastriate areas such as V3 which has a great number of cells tuned to the orientation of a stimulus, and area V5 which is dominated by cells selective for the direction of motion. Neither of these two areas has a large population of chromaticselective c e i l s 47"48~ Following the original demonstrations of a high incidence of wavelength-sensitive and colour-sensitive cells in a r e a V445-s~ several reports argued that the incidence of wavelength-sensitive cells was not particularly high and that cells in V1, V2 and V4 showed similar responses to chrotnatic stimuli9"z~176 Subsequent studies of the responses of cells in area V4 to chromatic stimuli extended the notion that populations of cells in V4 arc specialized for analyzing chromatic information. Zeki st'52 reported that some cells in V4 responded with 'colour constancy', that is, Correspondence: V. Walsh, Dept. of Experimental Psychology, University of Oxford, South Parks Rd., Oxford, OXI 3UD, UK.

tile response to a chromatic patch in a complex scene coincided with how the stimulus was perceived by a normal human observer regardless of the relative intensities of wavelengths reflected from the stimulus. Cells in V1 on tile other hand were reported to change their responses to a chromatic stimulus in register with the dominant wavelength reflected from the stimulus 5~'5z. A recent investigation of chromatic processing in V43~ has identified several interesting properties of neurons in this area. First, although V4 neurons seem to be no more narrowly tuned to wavelength than colour-opponent cells of the lateral geniculate nucleus (LGN), they have large receptive fields, often extending to the ipsilateral visual field, suitable for carrying out the summation of inputs from many thousands of LGN afferents over a large region of retinotopic space. Second, consistent with the computation of colour contrast, some V4 cells showed spectral selectivity for stimuli presented outside their classical receptive field. These properties arc necessary for the computation of colour constancy according to the rctinex theory of colour vision 17'53"5a. Third, unlike in the earlier stages of chromatic processing, carried out in arcas VI and V2, about 30~o of V4 neurons had two peaks of re-

52 sponse to wavelengths in different, though not necessarily opponent, regions of the spectrum. These are different from the end-spectrum double peaked cells in V1, the responses of which can be explained simply as a function of inputs originating in L- and S-cones 1~ In summary, then, the electrophysiological evidence shows that V4 neurons have chromatic response properties not seen in cells of other regions, which suggest that this area may have an important role to play in constructing and]or maintaining the perception of colour. There have been a number of behavioural studies of the effects of V4 lesions on colour vision. Dean 8 found that four monkeys with V4 lesions took longer than unoperated controls to relearn a pre-operatively acquired hue discrimination task but that their eventual thresholds were not elevated. At the time of Dean's experiments the population of wavelength-sensitive cells in the posterior bank of the superior temporal sulcus had not been reported46 and the possibility remained that th e sparing of hue discrimination thresholds was due to the survival of these ceils. Dean coneluded that "foveal V4 is not necessary for the discrimination Of small differences in successively presented hues". A similar conclusion was reached by Wild et al.43 who found that monkeys with partial V4 lesions, limited to the central and inferior visual field representation (see also ref. 4) could regain pre-operative levels of performance on a hue discrimination task but were impaired on a test ofcolour constancy. Thus it appears that hue discrimination can be performed if any of V4 remains intact but that the computation of colour constancy requires the integrity of the whole visual field representation. Heywood and Cowey 15 reported that two animals with complete V4 lesions and two animals with V4 lesions which extended into TEO were unable to regain their pre-operative level of performance on a hue discrimination task. However, these deficits, though persistent at small hue separations, were mild and there was much overlap between the V4 animals' pre- and postoperative performances (see fig. 4 of ref. 15). Subsequent studies have also reported very mild deficits of hue discrimination following lesions ofprestriate cortex which incorporate V416"31. Finally, Butler et al. 3 and Hilken et al. t7 observed a colour constancy deficit, but no hue discrimination deficit, in animals with lesions of V4. The experiments reported in this paper were undertaken to investigate whether monkeys with V4 lesions can regain pre-operative levels of hue discrimination performance and if they can perform a colour discrimination task which they find easy under one illuminant when the spectral content of the illuminant is changed.

The results show that area V4 is important for normal colour constancy performance, and that colour constancy deficits can be dissociated from hue discrimination performance. Parts of this work have been reported in abstract form37.

MATERIALS A N D M E T H O D S

Subjects Seven young adult rhesus monkeys were used. Full details of their training histories are detailed in another publication 36.

Surgery and histology Following completion of the tasks described in Expt. 2 of this paper, three monkeys (V4-1, V4-2, V4-3) received bilateral V4 ablations. Animal V4-4 took part in the post-operative testing in Expt. 3 only. Complete accounts of the surgical and histological procedures have been detailed elsewhere36. Briefly, the monkeys were anaesthetized with intravenously administered pentobarbitone sodium (0.6 mg/kg), and the lesions were made by sub-pial aspiration under aseptic conditions. The lesions were intended to include the prelunate gyrus from the junction of the intraparietal and lunate sulci. Both banks of the ascending arm of the inferior occipital sulcus were aspirated and an attempt was made to ablate the ventral projection described by Ungerleider35. Anteriorly, the lesions were intended to remove the lateral posterior bank of the superior temporal sulcus and, posteriorly, to remove the lateral anterior bank of the lunate sulcus. The animals were rested for 14 to 17 days post-operatively before retesting began. All made uneventful recoveries.

Apparatus and stbmdi The experiments were all carried out in the modified WGTA described elsewhere36. The WGTA was in a darkened room and for Expts. 1 and 2 the working area was ilIuminated by three projectors aligned to ensure that the working area was uniformly illuminated by" white light and that no coloured shadows could be formed by placing objects anywhere within the illuminated field. Light from each projector was filtered through one of three narrow-band filters: (Schott Glaswerke) 426.3 nm (half bandwidth 13.5 nm), 513.9 nm (half bandwidth 10.2 nm), and 613 nm (half bandwidth 13 nm). The intensity of light from each projector was determined by a variable transformer,

53 controlled by the experimenter. For Expt. 3, and the 'illuminance level' part of Expt. 2, the working area was illuminated by two 20 W fluorescent tubes (Thorn artificial daylight, colour temperature, 6,500 K). The stimuli were presented to the monkeys on a stimulus panel measuring 60 x 27 cm. This formed an angle of 60 degrees with the floor of the WGTA, with the upper edge of the panel furthest from the monkey. For Expts. 1 and 2 the board on which the stimuli rested was surrounded by a complex 'Mondrian' background which consisted ofcoloured squares and rectangles differing in size, hue, saturation and brightness (for examples see refs. 18, 24, 53, 54). For Expt. 3 the Mondrian was removed and the background was a uniform matte black. The stimuli, when placed on the board, were separated by a centre-to-centre distance of 10 cm. The lower edge of the stimulus plaques rested in a 'ditch' 8 mm deep and the plaques were secured at their upper edg~ by two hooks which prevented the animals from removing the stimuli from the background. To obtain a reward, therefore, the stimuli had to be displaced laterally away from the centre of the board. For Expt. 1 (hue discrimination) two sets of Munsell swatches were used. These were: Set 1: 7.5YR, 5R, 10R, 2.5YR, 5YR, 10YR, 2.5Y, 5Y, 7.5Y, 10Y, 5RP. Set 2: 10P, 10PB, 2.5P, 5P, 7.5P, 2.5RP, 5RP, 7.5RP, 10RP. In Set 1 the positive stimulus was 7.5YR and in Set 2 the positive stimulus was 10P. For Expt. 2 (colour constancy), subsets of stimuli from the two sets used in Expt. 1 were selected. These were: Subset 1: 7.5YR, 5R, 7.5Y. Subset 2: 10P, 10RP, 10PB. In these Subsets the positive stimuli were the same as in Sets 1 and 2. All stimuli were of Munsell Value and Chroma 6]4. Two examples of each stimulus were prepared. The swatches measured 75 • 55 mm and were mounted on aluminium plaques cut to the same size. They were covered by a sheet of non-reflective glass, also cut to the same size as the swatch, onto which margins of 1 cm were made by a textured, grey, matte tape. This border was changed after each day of training to prevent the monkeys from using any marks on the tape to identify the correct plate. The ditch in which the stimuli rested obscured the lower edge of the stimuli from the mon-

keys and, by alternating the position of the stimuli in this ditch, the animals were prevented from attending to any imperfections at the edges of the stimuli. The non-reflective glass was cleaned and checked for new dirt marks or scratches at the beginning of every training session and was in any event changed on a weekly basis. Munsell stimuli are calibrated for use under illuminant C (colour temperature 6,740 K), therefore precautions were taken to ensure that the animals had to learn the tasks by attending to the hue of a stimulus and not to any unintended cues caused by the brightness and saturation changes which occur When Munsell standards are presented under 'non-standard' conditions. Under the illuminant used here the Munsells appeared slightly more red and desaturated than when viewed under artificial daylight. Three measures were taken to ensure that the animals responded to the hue of the discriminanda. First, two naive human subjects were asked to rank the stimuli of both Sets in a colour sequence under daylight conditions and under the experimental illuminant. There was no difference between the two sequences in either of the two colour regions reported here. Second, to control for any lightness cues the monkeys might attempt to utilize, a 1 0 ~ neutral density filter was placed between the Munsell swatch and the non-reflective glass on one of each pair of stimuli and the two subjects were asked to rank the stimuli in order of apparent brightness under daylight and experimental conditions. In neither of the two sets of stimuli was there any correlation between hue and brightness. Third, when monkeys reached criterion in Expt. 1 it was found that the number oferrors made for each stimulus was related to its distance from the positive plate in terms of hue. During the course of a subsequent experiment39, the animals were given a two-choice discrimination task in which the discriminanda differed both in hue and luminance. They appeared to ignore the luminance difference and their responses could be understood only on the basis of hue differences, a finding possibly attributable to the experience gained during the experiments reported here. One can be confident therefore that the animals were responding to the hue of the stimuli presented here. A third set of stimuli was chosen for the postoperative, two-choice discrimination tasks of Expt. 3. These were four pairs of stimuli in which the first named is the positive plate and the second the negative plate. Set 3: (1) 7.5PB 4/12 vs. 8.75PB 4/12 (2) 2.5R 4/12 vs. 1.25R 4/12. (3) N5.25 vs. N5.75. (4) 8Y 5:12 vs. 8Y 5/14.

54 The stimuli in the first two pairs of Set 3 differ in hue, those in the third pair in reflectance, and the fourth pair in saturation. Procedure General The order of the experiments was as follows. Each animal was trained on a hue discrimination task with the stimuli from Set 1. The animals were then tested on the colour constancy task with stimuli from Subset 1. This order was then repeated for Set 2. On completion of the colour constancy task with stimuli from Subset 2 three of the animals received bilateral V4 lesions. Following recovery from the lesions the animals were retested on a series of shape discrimination tasks 36 before retesting commenced on the tasks reported here. Expt. 3 was conducted post-operatively only, after retesting on Ex'pt. 2 was completed. Testing w~is carried out 6 days a week. The monkeys were sophisticated at two-choice discrimination experiments and were familiar with the apparatus, therefore no preliminary training was given. A trial was carried out as follows. Two discriminanda were placed over the foodwells and the door between the monkey and the discriminanda was opened by the experimenter. If the animal's response was to remove the correct plaque it was allowed to retrieve a small food reward from the well. If the response was incorrect the screen was closed immediately. The position of the positive plaque was randomized for each trial, no position being rewarded more than three times in succession. The order of presentation of the negative plaques was also randomized. Intertrial interval was approximately 10 s. Masking noise was present during the trials. Experiment I: hue discrimhlation The monkeys were given sixty trials per day with the stimuli from Set 1 and were rewarded for displacing 7.5YR. Each of the negative hues was presented six times during a session. Criterion was set at 80~o correct over 150 trials consisting of fifteen presentations of each negative hue. With Set 2 the monkeys received sixty-four trials per day and were rewarded for displacing the 10P plaque. Each of the negative hues was presented eight times during a daily session. Criterion was set at 80~o correct over 160 trials consisting of twenty presentations of each negative hue. Experiment 2: colour constancy The ratio of light from the three projectors reflected by the six stimuli in the two Subsets was measured (PR 1,500 Spot Photometer). By adjusting the settings on

the variable transformer it was possible to make any negative plate reflect the sameratio of light from the three projectors as either the positive plate or the other negative plate reflected under the training illuminant. Two conditions were used. In the first condition, which we shall term S H I F T 1, the intensity of each of the projectors was changed such that a negative stimulus reflected the same amount of light from each projector as the positive stimulus had under the training illuminant. In the second condition (SHIFT 2), the intensity of the three projectors was changed such that a negative stimulus reflected the same amount of light from each projector as the other negative stimulus had under the training illuminant. These shifts are represented schematically in Fig. 1, and the reflectance ratios of the stimuli under the baseline conditions are given in Table I. If the lesioned animals behaved like photometers and responded only to the wavelength content of the stimuli then S H I F T 1 trials should produce a reversal in colour preference. The S H I F T 2 trials should produce either a chance performance since there is, photometrically at least, no positive plate in the array, or a preference for the positive plate which will reflect ratios closer to the training positive than the negative plate. Testing with the Subsets, in the order described above, proceeded as follows. The animals received sixty trials a day, 6 days a week until a criterion of 9 0 ~ correct over i00 trials was achieved. Training then continued as before but every daily session of sixty trials now contained twelve double-baited probe trials in which the relative intensities of the three projectors were changed and in which the animal was rewarded for displacing either of the two stimulus plaques. This double-baiting procedure was intended to prevent the

Fig. 1. Illumination shifts: the central plaque is the positive plaque and the direction of the illumination changes are indicated by the arrows. The solid lines represent illumination changes which we call SHIFT 1, and the dashed lines represent changes which we call S H I F T 2. For example, in the S H I F T 1 condition of Subset 1, the negative stimulus 5R would reflect the same ratios of long, middle and short wavelength light as the positive stimulus 7.5YR had reflected during Expt. 1 and the non-probe trials of Expt. 2. Similarly, in the S H I F T 2 condition of Subset 2 the negative stimulus 10PB would reflect the same ratios of long, middle and short wavelength light as the negative stimulus 10RP had reflected during Expt. 1 and the non-probe trials of Expt. 2. The baseline reflectance ratios of the stimuli under the training illuminant, are shown in Table I.

55 TABLE 1

Reflectances of the stbmdi used m the probe trials of Expt. 2 Each value given is a ~ a g e of the total luminance. Neutral density filters (0.1 log units) were used to randomize the brightness. The 'Total' row gives the luminance value of the stimulus paper, without the neutral density filter, in candelas per m-'.

Long Medium Short Total

l.ong Medium Short Total

7.5 )'R

5R

7.5 Y

6.0 86.5 7.5 4.0

7.7 81.1 11.2 3.4

5.6 88.5 5.9 5.6

lOP

IORP

IOPB

5.2 85.1 9.7 4.7

6.4 84.5 9.1 4.6

3.7 90.0 5.4 5.2

animals from learning to displace the correct plaque under the changed illutnination conditions since this would effectively have presented them with a new wavelength discrimination task and thus yielded no information on colour constancy. The order of presentation of the probe trials was randomized. A daily session of constancy probes consisted of six trials with each negative stimulus which in turn were made up ofthree trials in the S H I F T 1 condition and three trials in the S H I F T 2 condition. Probe trials were continued until the animal had received sixty probes with each Subset on days when the performance on the forty-eight normal trials was maintained at 90~o correct or better. At the end of the probe trials each animal had received 30 S H I F T 1 and 30 S H I F T 2 trials with each Subset of stimuli. To test whether the effects observed in the constancy task could be accounted for simply in terms of changes in the overall level of illumination, a control task was introduced. The animals were retrained to discriminate the stimuli in Subset 1 under two fluorescent tubes (Thorn Artificial Daylight). When a criterion of 9 0 ~ correct over 100 had been reached, probe trials were introduced in which the discriminanda were illuminated by only one of the tubes, yielding an illumination decrcmcnt of 50~/o, and an increment of 100~ when the second tube was reintroduced. These illumination changes are many times larger, and perceptually tnore salient, than any illumination changes in the probe trials. The anilnals received 30 probe trials under this condition.

EaTerhnent 3: hue, greyness aml saturation discrhnination On completion of the post-operative retesting of Expts. 1 and 2 the animals were tested on the four

two-choice discrimination pairs of Set 3. The animals received fifty corrected trials per day 6 days a week to a criterion of 90 correct responses over 100 consecutive trials or for a inaximunl of 500 trials on each discrimination.

RESULTS

Histology Full reconstructions of the lesions and assessments of the extent of L G N degeneration have bccn published elsewhere 36. The lesions were largely as intended and the only systematic departure from the intended site was the failure of the lesions to extend as far along the ventral projection as desired.

E.~7)eriment 1: hue discrimhmtion All three of the V4 animals regained pre-operative levels of performance on Set 1, and two ofthe lesioned animals regained criterion on Set 2. Fig. 2 shows the pre- and postoperative hue discrimination curves for the two groups of animals o11 Sets 1 and 2. It is clear that there are no differences between the groups after criterion has been achieved. The curves of the V4 group for Set 2 are taken from two animals since V4-3 failed to reach criterion in 3,000 trials and was withdrawn

B ~ ~l

100

10o80~"

6(}80 ~.'tt ~veJ17Y 3R ' V-Ipr~-op V4 po'~.op

40

t 2.5

t t 5 7.5

40

I

I

2.5

10 12.5

flueSteFs

=

I

I

5 7.5 I lae

-- -

!

1

10 12.5 Stc~s

100 %

so C ( ~ V

vI 40

.

Cont Fre.op Cont l~ost.op

----

I

I00

60

60

t

Set 2 . + ~ e = 10P v 4 Irre.cp V4po~-op

80 i.+re=10P

60

Coet Fr~-op Cont Fo~t o p

----

1

l

I

I

2.5

5

7.5

10

HuS e:eps

40

- -

!

I

I

!

2.5

5

7.5

10

H.:eS:eps

Fig. 2. Wavelength discrimination curves obtained in l-xpt. I. The dashed lines represent pre-operativc levels of performance and the solid lines the post-operative performances of the animals. A and C: lesioned animals. B and D: control group.

56 TABLE II

TABLE 111

Ire- and post-operative trials and errors f o r discrimhmtion Sets 1 aml 2 bt Expt. I ~ wavelength discrimhtation

Errors made on the two S I I I F T conditions hi each Subset

The saving scores for trials and errors are given in parentheses. Task

Sub

Pre.op

Post-op (savings)

Trials

Errors

C-I C-2 C-3 V4-I V4-2 V4-3

310 580 520 1240 910 630

102 202 170 360 256 125

C-I C-2 C-3 V4-1 V4-2 V4-3

512 624 336 320 396 344

147 172 98 67 83 105

Trials

Errors

Set 1

7.5YR 7.5YR 7.5YR 7.5YR 7.5YR 7.5YR

240(12.7) 320 (28.8) 240 (36.8) 580 (36.3) 360 (43.3) 420 (20)

51 (33.3) 94 (36.5) 65 (44.7) 196 (29.5) 121 (35.8) 89 (16.8)

Set 2

10P 10P 10P 10P 10P 10P

480 (3.2) 412 (20.5) 256 (13.5) 591 ( - 29.7) 556 ( - 16.8) 3000 **

81 (28.9) ! I1 (21.6) 79 (10.7) 351 ( - 67.9) 212 ( - 43.7) ** **

from further testing (see Discussion). Table II shows the number of trials and errors made during the acquisition and relearning of the hue discrimination tasks, and also shows the saving scores of each animal. There were no significant differences between the saving scores for either trials or errors on Set 1 ( M a n n Withney, U = I, nl =3, n 2 = 3, NS in both cases), but all the V4 animals did require more trials postoperatively than any of the control animals (U = 0, nl = 3 , n2 -- 3, P < 0.05) and two ofthe V4 animals also made more errors than any of the controls, though the number of errors made postoperatively did not differ significantly at the group level ( U = 1, n l = 3, n2 = 3, NS). On Set 2 the V4 animals required more trials post-operatively to reach criterion than any of the control animals ( U = 0 , nl = 3, n 2 = 3, P<0.05), they also made more errors than the control animals ( U = 0, nl = 3, n 2 = 3, P < 0 . 0 5 ) and the saving scores of the lesioned animals were worse for both trials and errors ( U = 0 , nl = 3, n 2 = 3, P < 0 . 0 5 in both cases).

Experiment 2: colottr constancy Table 11I shows the number of pre- and postoperative errors made on the 30 S H I F T 1 and 30 S H I F T 2 probe trials in each of the two subsets. Post-operatively, all the V4 animals made more errors than the control subjects on Subset 1 ( U = 0 , nl =3, n 2 = 3 , P<0.05), and the two V4 animals who completed testing on Subset 2 were also worse than the controls. Fig. 3 shows the total number of errors made over all probe trials.

In each column the first figure indicates the number of errors made pre-opcratively during thirty probe trials and the number in parentheses gives the number of errors made during post-operative retesting. For example, in the S I I I F T 1 condition of Subset I (when the reflectance ratios of stimulus 5R would be shifted to the ratios of 7.5YR during the non probe trial), animal V4-1 made one error pro-operatively and eight errors post-operatively. ** indicates that animal V4-3 was not tested post-operatively (see Discussion). Subset I

Subset 2

StHFT I

SIIIFT 2

SIIIFT 1

Sllll-'r 2

V4-1 V4-2 v4-3

5 (7) 5(10) 8 (12)

1 (8) 6(9) 9 (16)

4 (9) 2(11) **

2 (I I) 3(6) **

C-! C-2 C-3

4(3) 5 (5) 4 (5)

9(5) 5 (5) 1 (5)

4(4) 6 (4) 5 (4)

1 (4) 5 (4) 5 (2)

The total number oferrors made by each ofthe lesioned animals post-operatively was greater than that made by any of the controls ( U = 0 , h i = 3 , n 2 = 3 , P<0.05). There were no group differences on the saving scores over the total number of probe trials ( U = 1, n l = 3, n2 = 3, NS) but this is because the savings score measure exaggerates minor differences in performance when few errors are made. Also shown in Fig. 3 are the errors made in the Illuminance levels test of Expt. 2. I00~ m

75%

m

50%

25%

V4-1

V4-2

V4-3

Operated

I-I

C-I

C-2

C-3

Controls

I-I

I

Fig. 3. Comparison of percentage correct responses made pre- and post-operativcly over all constancy probe trials (n = 120) and the errors made post-opcratively in the lllunfination Level changes of Expt. 2 (, = 30).

57 NS), and all the V4 animals made fewer errors when the illumination level was changed than when the spectral content of the illuminants was changed (U = 0, n 1 = 3, n2 -- 3, P<0.05). In order to be tested on the probe-trials the animals had to reach 90/100 correct on each of the Subsets and in order to have the probe-trial scores of any given day included the animals had to maintain a performance of 90~o correct on the non-probe trials presented on that day. The errors made pre- and post-operatively by the animals in reaching 90/100 in the preprobe trial phase are shown in Table IVA and the number oferrors made pre- and post-operatively on the normal trials on the days when probe trials were given are shown in Table IVB. The V4 animals made many more errors than the controls post-operatively in reaching 90/100 correct on the two Subsets ( U = 0 , n l = 3 , n 2 = 3 , P < 0 . 0 5 ) and after reaching criterion the V4 animals also made more errors on the normal trials into which the probes were inserted ( U = 0, n 1 = 3, n2--3, P<0.05). However, on the days when probes were included for analysis there was no significant difference between the scores on the normal trials ( U = 1, n 1 = 3, n2 = 3, NS).

TABLE IV

Ire- and post-operative errors(A) to 90% on Subsets 1 and2, and(B) errors made on the normal trials over the days during which probe trials were administered in Expt. 2 These scores include the errors made on days when the animals failed to maintain 9 0 ~ correct and thus on days when probe trials were not included for analysis. Postoperative scores are in parcnthcscs. In Subset 2 ' F ' indicates that animal V4-3 was not tested due to failure to reach criterion in retesting (see Discussion).

elnhnal

Subset I

Subset 2

T A B L E IVA V4-1 V4-2 V4-3 C-1 C-2

9 (116) 32 (38) 48 (73) 24 (15) 23 (14)

26 40 4 42 33

c-3 TABLE IVB V4-1 V4-2 V4-3 C-I C-2 C-3

(63) (11 I) (F) (5) (12)

5 O)

20 (7)

9 (33) 56 (51) 11 (59) 43 (7) 23(14) 2 (9)

20 (23) 26 (42) 15 (F) 20 (11) 15(15) 13 (9)

E x p e r i m e n t 3: hue, g r e y n e s s attd saturation d i s c r i m i n a t i o n

Changes in illuminance levels did not produce differences between the two groups ( U = I, n l = 3, n2 = 3,

Table V shows

the number

animals on the acquisition

of errors made

of four two-choice

by the discrim-

TABLE V

The nunlber of errors, over six different c~terion levels, made b)' the anhnals on the acquisition of four two-choice discrimhlations hz Expt. 3 A: hue discrimination, 2.5R vs. 1.25R. B: hue discrimination, 7.5PB vs. 8.75PB. C: saturation discrimination, 8Y 5/12 vs. 8Y 5/14. D: greyness discrimination, N5.25 vs. N4.75. * indicates that the animal did not reach the designated level.

A

B 2.5R 4/12 vs. 1.25R 4/12

7.5PB 4/12 vs. 8.75PB 4/12

Animal

10]10

27[30

45/50

75/100

V4-1 V4-2 V4-4 C-I C-2 C-3

21 19 171 58 51 35

59 45 204 65 60 35

* * * 67 62 35

84 68 214 67 69 40

801100 * * * 67 71 40

90/100

Anbnal

10]10

27/30

45[50

75/100

80/100

90/100

II5F 165F 218F 79 71 43

V4-1 V4-2 V4-4 C-I C-2 C-3

32 9 24 7 111 18

76 9 9 8 113 162

* 9 * 8 114 163

94 , 78 17 114 32

* * * 19 116 *

192F 165F 198F 19 118 163F

75/I00

80/100

901100

C

D 8Y5/12 vs. 8Y5/14

Anhnal V4-1 V4-2 V4-4 C-I C-2 C-3

10/10

27]30

15 30 29 11 27 12

27 30 40 11 52 12

N5.25 ~. N4.75 45[50 63 46 49 12 61 12

75]100 45 33 72 15 59 21

801100 48 49 115 15 61 23

90/100 91 72 133 15 61 23

Anbnal V4-1 V4-2 V4-4 C-1 C-2 C-3

10/10

27/30

45/50

9 12 46 33 31 27

11 29 60 34 46 30

53 29 67 47 54 36

24 40 60 47 54 36

61 71 61 47 54 36

72 80 II6F 47 54 42

58 inations over five different criterion levels. On the two hue discrimination tasks (Table VA,B) the V4 animals reached a level of 10/10 in as few errors as the control animals ( U = 1, n 1 = 3, n2 = 3, NS, for each discrimination pair) and in both of the hue discriminations some overlap in the group performances is observed at 27/30 correct and 75/100 correct ( U = 1, nl -- 3, n2 = 3, NS, in all four cases). The V4 animals made more errors than the controls at all subsequent levels measured ( U = 0 , ill =3, n 2 = 3 , P < 0 . 0 5 in all six cases) and on neither of the hue discriminations did the lesioned group reach 45/50, 80/100 or 90/100 correct responses in the maximum number of trials allowed. On the saturation discrimination task (Table VC) there were no significant differences between the two groups at any of the five levels of performance measured prior to 90/100 correct ( U = !, n 1 = 3, n2--3, NS in all five cases) but in attaining the 90/100 correct level the animals in the lesioned group, who all reached this level, each made more errors ~than any of the controls ( U = 0, n l = 3, n2 = 3, P < 0.05). For the greyness discrimination task, Table VD shows that the V4 group performed as well as the controls at the 10/10, 27/30, 45/50, 75/100 levels of criterion ( U = 1, n l = 3, n2 = 3, NS in all four cases) but that the V4 group made more errors at the 80/100 ( U = 0 , n l = 3 , n 2 = 3 , P < 0 . 0 5 ) and 90/100 (U = 0, n 1 = 3, n2 = 3, P < 0.05) criterion levels. For each of the tasks in Table V, the number of errors made in reaching 10/10 correct were calculated as a percentage of the total number of errors made in that task. These figures are shown in Table VI. In each case the number of errors made in reaching 10/10 as a percentage of the total number made was greater for the controls than for the lesioned animals. There are two apparent exceptions to this. Animal V4-4 made a high proportion TABLE VI

The fltdivldual and mean number o f errors made in reachhtg 10]10 correct expressed as a percentage o f the total ntonber o f errors made ht reach#tg 90/100 correct on the four two-choice discffmination tasks ht Expt. 3 *** indicates that animal V4-2 did not achieve 10/I0 correct.

2.5R

8.5PB

8Y

N5.25

V4-1 V4-2 V4-4 V4-~

18.26 11.5 78.4 36.19

16.66 *** 12.12 14.39

16.48 41.66 21.8 26.65

12.5 15 39.66 22.39

C-1 C-2 C-3 C-X

73.4 71.8 81.39 75.53

36.8 94.06 11.04 47.3

73.33 44.26 52.17 56.58

70.1 57.1 64.8 63.97

of errors in reaching 10/10 on 2.5R vs. 1.25R, but this is a function of the large number of trials taken to reach 10/10 as a proportion of the maximum number of trials allowed. The other exception is animal C-3 who made only 11.04~o of the total errors to reach 10/10 on 7.5PB vs. 8.75PB.

DISCUSSION

The results demonstrate clearly that V4 lesions disrupt colour constancy in the absence of simple hue discrimination deficits. Moreover, the constancy deficits were obtained with stimulus pairs that the animals found very easy to learn to discriminate under a constant illuminant. 1,'4 and hue discrimblation The results of the hue discrimination tests (Fig. 2) demonstrate that animals with V4 lesions are able to regain pre-operative levels of performance on a hue discrimination test. The exception here is animal V4-3, an experienced working animal who, during the retesting on the Set 2 discriminations, became lethargic, lost fur from her coat, lost her appetite and failed to show her usual interest in the discrimination tasks. When she recovered, and was introduced to other tasks several months later, her discrimination abilities also improved. It seems likely, therefore, that her post-operative performance on the Set 2 tasks was more likely due to her illness than to the effects of the V4 lesion: the ablation did not differ in any major respect from that in the other animals. It is clear that relative to the unoperated animals the V4 animals take longer to relearn the discriminations. Having learned them, it is clear that they found it difficult to maintain a high level of performance. For example, on reaching 8 0 ~ over 150 or 160 trials the animals had usually reached 90~o correct or better on the largest of the hue separations within the two Sets of stimuli (Fig. 2) but when required to continue to perform at 90 ~o correct, during the overtraining which preceded the probe trials (Table IVA), the V4 animals made more errors than the controls. This observation was mirrored in the performance of the V4 animals during the probe trial days, when the lesioned group also made more errors than the normal animals on the non-probe trials (Table IVB). This erratic performance occurred at hue separations many times larger than the animals were capable of learning to discriminate. It is interesting to compare these relearning scores with the post-operative acquisition scores of the animals on the four two-choice discrimination tasks of Expt. 3 (Table

59 V). The V4 animals are impaired on the two hue discrimination tasks at the criterion level of 90]100, but they did perform as well as the controls at lower criterion levels (e.g. 27130), and two of the V4 animals reached 751100 on all four of the discrimination tasks. The problem for animals with V4 lesions therefore seems to be one of maintaining a high level of performance rather than of discrimination per se and it would be legitimate to interpret the performance of the V4 animals in Expt. 3 as evidence of slow learning. As the data in Table VI demonstrate, by the time a normal animal had reached 10]10 correct it had made over half the total number of errors, but by the time a V4 animal had reached 10]I0 correct, it had made only a small percentage ofthe total number of errors. However, slow learning cannot account for the errors made by the V4 animals on the simpler discriminations of Expt. 2 (Table IV), on which discriminations the animals had already achieved 9 0 ~ lzorrect over 100 trials before the probe trial schedule was introduced. This aspect of performance following prestriate lesions has been noted in other experiments in the context of acquiring a serial reversal discrimination task s and also in a probe-trial situation, similar to the one employed in the experiments reported in this paper, in which it was necessary for animals to maintain a high level of discrimination performance 4~. These data help to explain one aspect of the apparent contradiction between the results of Wild et al. 43, who stated that animals with V4 lesions did not have hue discrimination deficits, and the report by Heywood and Cowey ~s that animals with V4 lesions (with some intrusion into TEO) did have hue discrimination deficits. Wild et al. 43 did not obtain hue discrimination deficits because only the discrimination thresholds of the animals were considered and the criterion for threshold was 27/30 correct, a criterion V4 animals can achieve. The number of errors made in reaching that level of performance was not analyzed. The number of errors was taken into account in the latter study ~5 and there, as in this study, relearning but not threshold deficits were observed. These patterns of behaviour are unlikely to be the result simply of the removal of neurons that determine wavelength discrimination thresholds, for which adequate resources can be found in areas VI and V21~176 because the impairment of the animals was in performing at a consistently high level and not in reaching the criterion in the first place. Rather, they are better explained as a consequence of the removal of V4 cells involved in more complex aspects of processing such as selective attention. For example, Spitzer et al. 32 found that V4 neurons increased their firing rate and selectivity when a colour matching

task was made more difficult. It is worth noting therefore that selective attention to different aspects of colour stimuli can yield changes in similarity judgemerits 33. It may be, then, that monkeys with V4 lesions adopt different attentional strategies than normal monkeys, have difficulty selecting a single strategy from those available or are unable to sustain their attention over a large number of trials (a phenomenon also observed in patients with visual neglectS4). V4 attd colour constancy The results of Expt. 2 replicate and extend our previous finding 43 that normal monkeys, like goldfish 18, honeybees 42 and humans 22"23, can identify surface cotours despite changes in the ratios of wavelengths reflected from them, but that monkeys with V4 lesions are impaired. Two of the animals with V4 lesions made fewer than 75~o correct judgements over the constancy trials (Fig. 3), and the constancy abilities o f o n e animal, V4-3 were reduced to chance levels (Fig. 3). The finding that V4 lesions produce constancy deficits can be predicted from the elcctrophysiological and ncuro-imaging evidence that V4 is involved in higher order colour processing 7'29'49"sl'52`sS, and from earlier behavioural studies which have found constancy deficits following V4 lesions 3'43. It has been argued that if wavelength discrimination is impaired, then "colour constancy can hardly be normal" (ref. 56, p. 203). The data reported here contradict this view since deficits were obtained with stimuli the monkeys found easy to discriminate under the training illuminant. We also excluded the possibility that the difficulty in maintaining a high level of performance could account for the constancy deficits observed, since, to ensure that the performance of the animals on the constancy probe-trials could not be explained as a function of a non-specific decrement in discrimination abilities, constancy was only assessed on days when the animals did not display a difficulty in maintaining a high level of performance (see Materials and Methods). There is also good reason to dispute the logic of the statement that if there is a wavelength discrimination deficit there is necessarily a constancy deficit. This is analogous to arguing that all low level deficits (e.g. raised visual acuity thresholds) necessarily entail higher order deficits such as gross shape discrimination or recognition deficits - of course, they do not 4~ It is well recognized that constancy is not a precise computation but an approximate one in which a colour retains membership of a perceptual category 2~a2"38. Since there are only eight suprathreshold chromatic categories which cover colour identification and memory throughout colour space t'2 and even fewer

60 at detection threshold 25 it seems improbable that small wavelength discrimination deficits would affect either colour categorization or colour constancy 2~'39. There are reasons why the effects of V4 lesions on colour constancy may have been underestimated by the methods used in Expt. 2. The animals were retested on the tasks reported here after being retested on a series of two-choice shape discrimination tasks 36. Thus the deficit was persistent over a period of several months, in contrast with the short-lived deficits following lesions to other regions of prestriate cortex such as the motion area 8'26'z7. Indeed we have observed colour constancy deficits to persist for over a year in animals with only partial lesions of V44. In a natural setting, constancy is often achieved with time delays between presentation and identification of the stimulus, under conditions in which the location of the target colour and the direction of the illuminant are changed, and against a background of changing Spatial and temporal information. Schiller and Lee 31 have shown that animals with V4 lesions are poor at transferring acquired visual discrimination skills to any kind Of new context. In the present study, the spatial configuration of the discriminanda and the multi-coloured surround were unchanged throughout. Further, the stimuli were always illuminated from above and there were no distracting shadows in the experimental setting. One would predict, then, that monkeys with V4 lesions would have greater constancy deficits if tested for constancy under conditions in which the location of the positive stimulus was varied across a greater number of spatial locations; when the spatial and chromatic content of the Mondrian surround was varied; and when the direction of the illuminant and shadow configurations were manipulated in tandem with spectral changes. Indeed it has been demonstrated that changes in shadow configurations alone are sufficient to disrupt perception in monkeys with prestriate cortical lesions 41. One referee of this paper asked whether the monkeys could have adapted to the probe trials by learning the rule 'change in illuminant means that any stimulus is rewarded'. There is good evidence that this is not the case: the changes in the constancy probe trials were difficult to detect; the use of neutral density filters prevented the monkeys from using lightness as a cue to the direction of change; there was no greater decrement in performance in the Shift 2 probe trials when the illuminant shift was greater than in the Shift 1 trials; there was no apparent transfer of such a rule to the task in which the intensity, but not the spectral content of the incident illumination was changed; and the monkeys did not make errors when the illuminant was shifted back from the probe condition to the training condition.

Finally it is important to note that the constancy deficit has also been obtained in a single-baiting procedure 43. Area V4 is not the only site implicated in colour constancy. Several commentators have emphasized the importance of photoreceptor adaptation in discounting the illuminant, and this clearly has a role in colour vision (see ref. 38). However, as Pokorny et alfl 8 state "There is clear evidence against the view that constancy is mediated entirely.., at a peripheral site" (p. 55). The results presented here can be added to that body of "clear evidence". A final point of interest is the question of how the contribution of V4 to the analysis of colour relates to the chromatic processing carried out in other visual cortical areas. Electrophysiological and behavioural evidence suggests that basic colour categories are formed in areas V1 and V2 (refs. 21, 39, 44; and Yoshioka, personal communication), and it is to be expected that colour constancy is subject to category effects in the same manner as discrimination, naming and memory ~'2'2t'25'38. Colour processing that occurs after V4, in the inferotemporal cortex, is thus likely to be important for short-term colour memory ~1-13,19.

ACKNOWLEDGEMENTS

This work was partly funded by the Wellcome Trust. We are grateful to U M I S T Academic Resource and Development Fund, and The Department of Optometry and Vision Science and Professor John CronlyDillon for support which enabled the work to be completed. Thanks are due to Dr. D.I. Perrett for his comments on the MS, and two referees for suggesting several non-trivial changes to the text.

REFERENCES 1 Boynton, R.M., Fargo, L., Olson, C.X. and Smallman, tI.S., Category effects in colour memory, Colour Res. AppL, 14 (1989) 229-234. 2 Boynton, R.M. and Olson, C.X., Salience of chromatic basic colour terms confirmed by three measures, Vision Res., 30 (1990) 1311-1317. 3 Butler, S.R., Carden, D., ttilken, II. and Kulikowski, J.J., Deficit in colour constancy following V4 ablations in rhesus monkeys, J. Physiol., 403 (1988) 72 p. 4 Carden, D., Hilken, tI., Butler, S.R. and Kulikowski, J.J., Partial lesions of primate visual area V4 affect colour constancy, Irish d. PsychoL, in press. 5 Christensen, C.A. and Pribranl, K.II., The effect of inferotemporal or foveal prestriate ablation on serial reversal learning in monkeys, Neuropsychologia, 17 (1979) 1-10.

61 6 Collin, N.G. and Cowey, A., The effect of ablations of frontal eye fields and superior colliculi on ~Ssual stability and movement discriminationin rhesus monkey, Exp. Brabl Res., 35 (1980) 251260. 7 Corbetta, M., Miezin, F.M., Dobmeyer, S., Shulman, G.L. and Petersen, S.E., Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomo~aphy, J. NeuroscL, 11 (1991) 2383-2402. 8 Dean, P., Visual cortex ablation and thresholds for successively presented stimuli in rhesus monkeys. 2. Hue, Exp. Brahl Res., 35 (1979) 69-83. 9 De Monasterio, F.M. and Schein, S.J., Spectral bandwidths of color-opponent cells of gcniculocortical pathways of macaque monkeys, J. Neurophysiol., 47 (1982) 214-224. 10 Dow, B.M. and Vautin, R.G., Horizontal segregation of color information in the middle layers of foveal striate cortex, J. NettrophysioL, 57 (1987) 712-739. 11 Fuster, J., Inferotemporal units in selective visual attention and short-term memory, J. Neurophysiol., 64 (1990) 681-697. 12 Fuster, J. and Jervey, J.P., Inferotemporal neurons distinguish and retain behayiourally relevant features of visual stimuli, Science, 212 (1981) 952-955. 13 Fuster, J. and Jervey, J.P., Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task, J. NeuroscL, 2 (1982) 361-375: 14 Heilman, K., Unilateral spatial neglect, McDonnell-Pew Ne,troscience Sem#lars, 1992, Oxford. 15 Heywood, C.A. and Cowey, A., On the role of cortical area V4 in the discrimination of hue and pattern in macaque monkeys, J. Neurosci., 7 (1987) 2601-2617. 16 Heywood, C.A., Shields, C. and Cowey, A., The involvement of the temporal lobes in colour discrimination, Exp. Brahz Res., 71 (1988) 437-441. 17 Hilken, H.S., Carden, D. and Butler, S.R., Colour constancy in monkeys and humans. In J.J. Kulikowski, C. Dickenson and I.J. Murray (Eds.), Seeing Contourand Colour, Pergamon Press, 1989. 18 Ingle, D., The goldfish as a retinex animal, Science, 227 (1985) 651-654. 19 Komatsu, H., Ideura, Y., Kaji, S. and Yamane, S., Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey, J. Ne,lrosci., 12 (1992) 408-424. 20 Kruger, J. and Gouras, P., Spectral selectivity of cells and its dependence on slit length in monkey visual cortex, J. Neurophysiol., 43 (1980) 1055-1069. 21 Kulikowski, J.J. and Walsh, V., Colour Vision: isolating mechanisms in overlapping streams. In S. Molotchnikoffand T.P. Hicks (Eds.), Progress in Brahz Research, in press. 22 Land, E.H., Color Vision and the natural image: Part 1, Proc. NatL Acad. ScL USA, 45 (1959) 115-129. 23 Land, E.H., Color Vision and the natural image: Part 2, Proc. Natl. Acad. ScL USA, 45 (1959) 636-644. 24 Land, E.H., An alternative technique for the computation of the designator in the retinex theory of color vision, Proc. Natl. Acad. Sci. USA, 83 (1986) 3078-3080. 25 Mullen, K.T. and Kulikowski, J.J., Wavelength discrimination at detection threshold, J. Opt. Soc. Am. A, 7 (1990) 733-742. 26 Newsome, W.T., Wurtz, R.H., Dursteller, M.R. and Mikami, A., Deficit in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey, J. NeuroscL, 5 (1985) 825-840. 27 Newsome, W.T. and Pare, E.B., A selective impairment of motion perception following lesions of the middle temporal visual area (NIT), J. Neurosci., 8 (1988) 2201-2211.

28 Pokorny, J., Shevell, S.K. and Smith, V.C., Colour appearance and color constancy. In P. Gouras (Ed.), Vision and Visual Dysfunction, VoL 6: Colour Vision, Nlacmillan, 1991, pp. 43-61. 29 Schein, S.J. and Desimone, R., Spectral properties of V4 neurons in the macaque, J. Neurosci., 10 (1990) 3369-3389. 30 Schein, S.J., Marrocco, R.T. and De Monasterio, F.M., Is there a high concentration of color-selective cells in area V4 of monkey visual cortex? J. NeurophysioL, 47 (1982) 193-213. 31 Schiller, P.H. and Lee, K., The role of the primate extrastriate area V4 in vision, Science, 251 (1991) 1251-1253. 32 Spitzer, H., Desimone, R. and Moran, J., Increased attention enhances both behavioural and neuronal performance, Science, 240 (1988) 388-340. 33 Stalmeier, P.F.M. and de Weert, C.M.M., Large color differences and selective attention, J. Opt. Soc. Am. A, 8 (1991) 237-247. 34 Tanaka, M., Weber, H. and Creutzfeldt, O.D., Visual properties and spatial distribution of neurones in the visual association areas on the prelunate gyrus of the awake monkey, Exp. Brahz Res., 65 (1986) 11-37. 35 Ungerleider, L.G., The corticocortical pathways for object recognition and spatial perception. In C. Chagas, R. Gattass and C. Gross (Eds.), Pattern Recognition Mechanisms, Pontificae Academiae Scientiarum Scripta Varia No. 54, 1985, pp. 2139. 36 Walsh, V., Butler, S.R., Carden, D. and Kulikowski, J.J., The effects of V4 lesions on the visual abilities of monkeys: shape discrimination, Behav. Brain Res., 50 (1992) 115-126. 37 Walsh, V., Butler, S., Carden, D. and Kulikowski, J.J. Wavelength discrimination and colour constancy in monkeys with V4 lesions, Perception, 20 (1991) A54. 38 Walsh, V. and Kulikowski, J.J., Seeing colour: the nonNewtonian brain. In R. Gregory, D. Rose, J. Harris and P. Heard (Eds.), The Artful Brahs, O.U.P., in press. 39 Walsh, V., Kulikowski, J.J., Butler, S.R. and Carden, D., The effects of V4 lesions on the visual abilities of monkeys: colour categorization, Behav. Brain Res., 52 (1992) 81-89. 40 Warrington, E.K., Visual deficits in associated with occipital lobe lesions in man. In C. Chagas, R. Gattass and C. Gross (Eds.), Pattern Recognition Mechanisms, Pontificae Academiae Scientiarum Scripta Varia No. 54, 1985, pp. 247-261. 41 Weiskrantz, L. and Saunders, R.C., Impairments of visual object transforms in monkeys, Brain, 107 (1984) 1033-1072. 42 Werner, A., Menzel, R. and Wehrhahn, C., Color constancy in the honeybee, J. Neurosci., 8 (1988) 156-159. 43 Wild, H.M., Butler, S.R., Carden, D. and Kulikowski, J.J., Primate cortical area V4 important for colour constancy but not wavelength discrimination, Nature, 313 (1985) 133-135. 44 Yoshioka, T., Dow, B.M. and Vautin, R.G., Hue, luminance and hue/luminance cells in foveal V1, V2 and V4 of the behaving monkey, Soc. Neurosci. Abstr., 13 (1987) 177.2. 45 Zeki, S.M., Colour coding in the rhesus monkey prestriate cortex, Brain Res., 53 (1973) 422-427. 46 Zeki, S.M., Colour coding in the superior temporal sulcus of the rhesus monkey visual cortex, Proc. R. Soc. Lond. B., Biol. Sci., 197 (1977) 195-223. 47 Zeki, S.M., Uniformity and diversity of structure and function in the rhesus monkey prcstriate visual cortex, J. Physiol., 277 (1978) 273-290. 48 Zeki, S.M., Functional specialization in the visual cortex of the rhesus monkey, Nature, 274 (1978) 423-428. 49 Zeki, S.M., The representation of colours in the cerebral cortex, Nature, 284 (1980) 412-418. 50 Zeki, S.M., The distribution of wavelength- and orientation-

62

51

52

53

54

selective cells in different areas of monkey visual cortex, Proc. R. Soc. Lond. B, Biol. Sci., 217 (1983) 449-470. Zeki, S.M., Colour coding in the cerebral cortex: the reaction of cells in monkey visual cortex to wavelengths and colours, Neuroscience, 9 (1983) 741-765. Zeki, S.M., Colour coding in the cerebral cortex: the responses of wavelength-selective and colour-coded cells in monkey visual cortex to changes in wavelength composition, Neuroscience, 9 (1983) 767-781. Zeki, S.M., Colour vision and functional specialization in the ~Asual cortex, Discussions in Neuroscience, Vol. 6, Elsevier, Amsterdam, 1990. Zeki, S.M., Functional specialization in the visual cortex: the

generation of separate constructs and their multistage integration. In: J.C. Eccles and O. Creutzfeldt (Eds.), The Principles of Operation and Design of the Brain, Pontifical Academy of Sciences, Vatican City Press, 1991, pp. 85-130. 55 Zeki, S., Watson, J.D.G., Lueek, C.J., Friston, K.J., Kennard, C. and FrackoxHak, R.S.J., A direct demonstration of functional specialization in human visual cortex, J. Neurosci., 11 (1991) 641649. 56 Zrenner, E., Abramov, I., Akita, M., Cowey,.A., Livingstone, M. and Valberg, A., Color perception: retina to cortex. In: L. Spillman and J.S. Werner (Eds.), Visual Perception: Tile Neurophysiological ~bundations, Academic Press, London, 1990, pp. 163204.