PergamonVisionRes.,Vol.37,No.12,pp. 1581-1593,1997

@1997ElsevierScienceLtd.AUrightsreservedPII: S0042-6989(96)00320-3 Printedin GreatBritain

0042-6989/97$17.00+ 0.00

Simultaneous Color Contrast in Goldfish—a Quantitative StudySASKIA DORR,* CHRISTA NEUMEYER*~

Received 6 May 1996; injinal form 10 September 1996

A set of 9-15 colored test fields was presented to goldfish. In Experiment 1, test field hues rangedfrom green through yellow to red; in Experiment 2, the hues varied from blue through gray toyellow. In the training conditions, the test fields were presented with a gray or black surround. Thefish learned to choose one intermediate test field hue by rewarding them with food. In the testconditions, the color of the surround was changed from gray to green, or red (Experiment 1), andfrom black to blue, or yellow (Experiment 2). The choice behavior of the goldfish changedsubstantially: one of the test fields other than the training test field was preferred. Direction andstrength of simultaneous color contrast was quantified in goldfish color space. The effect of spatialstimulus configuration was investigated by changing test field size and using narrow annularsurrounds. With test field radii ranging between 2 and 7.5 mm simultaneous color contrast wasoptimal whenever the ratio between surround width and test field radius had a value of about 1:1.01997 Elsevier Science Ltd.

Simultaneouscolorcontrast Colorvision Goldfish Carassiusauratus

INTRODUCTION

The goldfishis especiallywell suited for investigationsofthe visual system because of a rare combination of twoproperties: it is very cooperative in behavioral trainingexperiments, and its retina can be investigatedrelativelyeasily with electrophysiologicalmethods (see for reviewDjamgoz& Yamada, 1990).The goldfishcan be regardedas a model system for the understandingof human colorvision. This view is mainly based on the findingsthat thehorizontal cells in the retina of cyprinid fishes reveal“color opponent” responses (Tomita, 1965), and “doublecolor opponent”cells are found in goldfishon the level ofbipolar and ganglion cells (Daw, 1967; Kaneko &Tachibana, 1981). Double opponent cells, which arediscussed in the context of simultaneous color contrastand color constancy, are found in primates only in thevisual cortex.

In training experiments it was shown that color visionin goldfish is even more complicated than human colorvision as it is tetrachromatic(Neumeyer, 1992)with threeranges of highest wavelength discrimination ability(Neumeyer, 1985, 1986; Fratzer et al., 1994).

To study the functional organization of color visionfurther, we have now investigated simultaneous colorcontrast. This phenomenon is relevant because it isprobably functionallyconnectedwith color constancy,an

*Institut fiir Zoologie III, Johannes Gutenberg-Universitat, 55099Mainz, Germany.

tTo whom all correspondenceshouldbe addressed [Fax +49/6131/39-5443;Email:christa.neumeyer@uni-maint.de].

ability shown in cyprinid fish (Burkamp, 1923; Diment-man et al., 1972; Ingle, 1985;Dorr & Neumeyer, 1996).Simultaneouscolor contrast is observed (in human colorvision) whenever a relatively small test field is seensimultaneouslywith an adjacent colored surround.Thenthe hue of the test field is altered to a hue complementaryto that of the surround(in the case of a gray test field) orto a hue “away” from surround when colored test fieldsare used (see for review Graham & Brown, 1965).Understrong fixation, or with very short presentation times ofthe surroundcolor the phenomenonmust be due to lateralinteractionsbetween the areas stimulatedby test field andsurround.Undernaturalviewingconditions,however, theeffect is influenced by successive color contrast, anaftereffect of chromatic adaptation, as noted by Helm-holtz (1911).

In contrast to the extensive studies in humans, only afew authors have investigated simultaneous color con-trast in animals:e.g., in primates (Grether, 1942;Brenneret al., 1988), chicken (Revesz, 1921), pigeons (Budnik,1985 cited in Varela et al., 1993) and some species ofteleost fishes (Herter, 1950).A qualitative and quantita-tive analysis of simultaneous color contrast wasperformed in an insect, the honeybee (Kuhn, 1927;Neumeyer, 1980). Here also successive color contrastwas shown (Neumeyer, 1981).

Herter (1950) investigatedsimultaneouscolor contrastin five different teleost species: two cyprinids (tenchTinca vulgaris Cuv., barb Barbus partipentazona Fow-ler), one cichlid (the Gill fish Hemichromis bimaculatusGill), the three-spinedsticklebacks(Gastrosteusaculeatus

1581

1582 S. DORR AND C. NELJMEYER

L.), and Pterophyllum eimekei E. Ahl. He presented twocolored test fieldssimultaneously,e.g. green and yellow–green, with a gray surroundand trained the fish on one ofthem. In the test situation,two gray test fieldswere shownwith differently colored surrounds, which, due tosimultaneous color contrast appeared to the humanobserver as similar to the colored test fields in thetraining situation. For example, the gray test field withred surround appeared greenish. Fish trained on a greentest field did indeed prefer the gray field combined withthe red surround, and not with the blue surround. Thiswas the first hint that simultaneouscolor contrast occursin fish.

We investigated simultaneous color contrast for twosets of colors (red–green, and blue–yellow), located ingoldfish color space on two different axes. Applyingcolor metrics, we quantifieddirection and strength of theinduced hue shift. We also investigated the effect ofvarying the spatial parameters of the stimulus.

MATERIALSAND METHODS

Rationale

A series of test fieldswith different hues, for example,hues varying from red over yellow to green, waspresented to goldfishwith a gray surround.The goldfishwere trained to approach an intermediateorange trainingfield by rewarding them with food. In the test situation,the same test fieIdswere presented to the goldfishbut thecolor of the surround was changed from gray e.g., togreen. We expected that the goldfishwould choose a testfield with a hue most similar to the hue of the trainingfield with gray surround.

If goldfish do not exhibit simultaneouscolor contrast,the test field colors will not be influenced by thesurrounding color and the fish would not change itschoice behavior. If, on the other hand, goldfishperceivesimultaneouscolor contrast, they will not recognize thetraining field because it (and all other test fields)appears“less greenish” (or “more reddish”) than in the trainingsituation. That is, the goldfish should choose anobjectively “more greenish” test field resembling thehue of the training field with gray surround. Thus,simultaneouscolor contrast can be measured as a shift inrelative choice frequency.This method has the advantagethat the original training field is always present. Ifgoldfish choose a different test field in the contrastsituation, there is no doubt that its hue matches thetrained hue‘betterthan the trainingfield itself in the givensituation. The variety of slightly different test field huesallows the fish to select that particular test field whichbest resembles the hue of the original training field.

Experimentswere performedwith two sets of test fieldhues: in Experiment 1, hues ranged from red over orangeto yellow–green, and in Experiment 2, from blue overgray to yellow. To quantify the results,.we characterizedthe test field colors for goldfishcolor vision by applyingcolor metrics.

(b)

FIGURE 1. (a) Goldfish tank in experimental set-up. View fromobserver’s position. (b) Side view of the tank and the illumination

device in Experiment 2 (see text).

Experimental set-up

The Plexiglas tanks (40 x25x 28 cm) were equippedwith a water filter unit and illuminated from above bywhite light.The test fieldswere presented simultaneouslyto the goldfish behind the rear panel of the tank [Fig.l(a)]. They were randomly distributed on a disk(diameter 23 cm) which could be rotated to avoidposition learning. The remainder of the rear panel wascovered with white paper. Two disks fixed to a rotatablerod so that they could be interchanged[cf. Fig. l(a)] wereused in the experiments. During pretraining, each diskwas covered with gray paper forming the surroundof thetest fields. In the experimentitself, one disk was coveredwith colored paper, the other one with gray paper. Thefish was observed from the front panel. A whitecardboard was placed between observer and front panelat a 45 deg angle to reflect the light from above onto thetest fields and to avoid disturbancesfrom outside.

In Experiment 2, the set-up differed in the followingway [Fig. l(b)]: the tank was placed in an experimentalchamber (not shown in the figure)that was covered withblack paper at the back and white paper at the sides.

SIMULTANEOUSCOLOR CONTRASTIN GOLDFISH 1583

R6R5R4R3R2RITG1G2G3

300 400 500 600 700wavelength [rim]

(c).

red

green

light gray

gray

//

Io~wavelength [nml

o~300 400 600 700

wavelength [rim]

(d)

~ yellow; 80-v bluec

block: 60-=2 40-al>.-jj~ 20-k

300 400 500 600 760wavelength [rim]

FIGURE2. Relative spectral reflectanceof papersused as test fieldsandsurrounds.(a) Test fieldsusedin Experiment1:R6-R1,red test fields; T, orange training field; G1-G3, yellow–greentest fields. (b) Test fields used in Experiment2: B6-B1, blue testfields;T, bluishgray trainingfield; Y1–Y8,yellowtest fields. (c) Surroundsusedin Experiment1. Gray: trainingsurround;red,green, light gray: test surrounds.(d) Surroundsused in Experiment2. Black: training surround;yellow, blue: test surrounds.

Black cardboard was used as a training surround insteadof gray paper. The same cardboard also covered the rearpanel of the tank. The opening left for the disk had adiameter of 22 cm. The differences in the two experi-ments occurred because Experiment2 was run in the set-up used for a quantitative analysis of color constancy ingoldfish (for details see Dorr & Neumeyer, 1996).

Testjields and surrounds

Experiment 1. The nine colors for the test fields,varying between red and green, were chosen from matHKS papers (H. Schminckeand Co). The orange trainingfield was named T, the more green test fields G1 to G3,the more red ones R1 to R6, corresponding to theirgreenness or redness for the human observer (T= HKS72; G1 = HKS 4; G2 = HKS 68; G3 = HKS 2; R1 = HKS6; R2 = HKS 7; R3 = HKS 81; R4 = HKS 8; R5 = HKS10; R6 = HKS 14). The gray training surround, red testsurround and white cover of the tank consisted ofcommercially available paper. HKS 69 paper was usedfor the green test surround.

Small disks with radii of 1.1 cm were stamped out ofthe paper for the test fields. This radius was reduced to0.75, 0.5, 0.3 or 0.2 cm for investigations of the sizeeffect. The coIored surround covered the whole disk in

the basic experiment or was reduced to a concentricannulusaroundeach test fieldwith outer diametersof 4.5,3.7, 3.0 and 2.5 cm.

Experiment 2. The 15 test field colors, varying fromyellow over gray to blue, were produced using a ColorPaintbrush Printer (HP Deskjet 500 C) and appropriatesoftware.They were printed on self-adhesivewhite paperand coated with mat protective lacquer against damageby water. The bluish trainingfieldwas named T, the moreyellow test fields Y1–Y8, the more blue ones B1–B6,ordering them according to the saturationas observedbyhumans.The test field radius was 0.7 cm and the coloredsurround covered the entire disk. Yellow and blue testsurround,white and black paper for coveringparts of thetank consisted of commercially available paper.

The spectral reflectance of each paper was measuredwith a double-beam spectrophotometer(Pye Unicam P1800UltravioletSpectrophotometer)from300to 750 nm.The values were related to the reflectanceof magnesiumoxide. In Fig. 2 the relative reflectance of the test fields[Fig. 2(a, b)] and surrounds[Fig. 2(c, d)] are shown.

Illumination

Experiment 1. The tanks were illuminated directlyfrom above by four daylight fluorescent lamps (Osram

1584 S. DORR AND C. NHJMEYER

0300 400 500 603 700

wavelength [rim]

FIGURE3. Relative spectral irradiance of the illumination.Columns:fluorescent lamp (L39W19 daylight deluxe, Osram) used in Experi-ment 1; continuousline: white light obtainedby additivecolor mixtureof three projectorswith blue, green, and red filter (SchottBG 12,VG6,

OG 590), respectively, used in Experiment2.

L39W/19, 5000 deluxe), with relative spectral radiantflux as shown in Fig. 3. The illuminance at the watersurface corresponded to about 300 lx, measured bydirecting the detector head of the photometer upwards(EG and G radiometer/photometer,type 550-1).

Experiment 2. The white light which illuminated theexperimental tank from above resulted from an additivemixture using three projectors (1 Leitz Prado Universal250 Watt, 2 Leica Pradovit P2000 250 Watt). Each lightsource was equipped with a differently colored broadband filter producing blue, green, or red light (SchottBG12, VG6, OG590).The projectorsilluminateda whitecardboardscreenwhich was fixedabovethe experimentalchamber at an angle of 45 deg [Fig. l(b)]. The spectralirradiance of light was measured in the spectral rangebetween 300 and 750 nm with a spectrophotometer(EGand G 550-1, combined with a monochromator systemEG and G 555-61M). The detector head was directedupwards at the water surface and located at the center ofthe tank. Figure 3 shows the spectral radiant flux.Additionally, we measured the light photometricallyand obtained about 40 lx.

Animals

Normally shaped and pigmented goldfish wereobtained from local dealers. The fish were namedindividually and the abbreviations of these names areused below to identifythem. They were kept separatelyin301 tanks at room temperature. During the experiments,fish were fed only during the training sessions or intraining sessionsbetween tests. In Experiment 1, trainingand testing of three goldfish(fishM., S., K.) took place intheir home tanks (40 x 25 x 28 cm). In Experiment2, fish(fish C. and G.) were carried from their home tank to theexperimental tank (in a plastic beaker). During theintervalsbetween the experimentsthe fish were fed withflake food.

Training and testingprocedure

The procedureof training and testingwas the same forthe two experiments. Before the experiments, the fish

were adapted to the illuminationin the set-up for at least10 min. At the beginning, the fish had to learn to “peck”at the training field presented with the gray or blacktraining surround covering the entire disk behind theglass panel. They were rewarded with a bit of food pasteeach time they approached the field. The food pasteconsisted of commercial fish food (Tetramin, Tetra)solubilized in water and thickened with Traganth(Merck).Vitaminswere added. The food paste was filledin a syringe and pressed into a plastic tube (innerdiameter 1.2 mm) fixed to a plastic stick. This “foodstick” was held by the experimenterwho could thus putfood at any location of the training field. After eachreward, the diskwas removed and, after at least 5 see, theother disk with a different arrangementof test fieldswaspresented.The diskswere shownalternatelyand revolveda varying number of degrees after each reward to avoidposition learning.

The pretraining was finished after the fish chose thetraining field at a constantly high level for at least 5consecutivedays. Obviously,the task was not easy. Mostgoldfishdid not learn to prefer the training hue. For theothers,whose results are presented here, pretrainingtookfrom a few weeks to monthsdependingon the individualfish. In experiment 1, fish K. learned it first. Fish M. andS. did not learn to discriminatetraining field T from (thevery similar) test fields R1 and R2. Therefore, these twotest fields were removed from the sample for these twogoldfish. Comparable problems occurred in Experiment2. Fish C. learned the task first, fish G. learned it withoutthe test fields B1 and G1 in the sample.

After the fish had learned the task, their choicebehavior was recorded with the (gray or black) trainingsurrounds. Each experiment (once per day, lasting forabout 1 hr) started with several “training sessions” tokeep the learning level constant, and as high as possible..Here, the first six “pecks” at any test field presented withthe ‘training surround were counted as choices andrecorded. Then, the fish were rewarded at the trainingfield. This was repeated about 10 times. In the “testsessions” for color contrast, the gray or black surround,respectively,was replaced by a colored surround, usingthe second disk. Again, the first six “pecks” of thegoldfishwere recorded.The reward was given only in thefollowing “intermediate training session” with thetraining surround after six choices. Then, the next “testsession”with colored surroundfollowed, and the rewardin the presence of the training surround, and so on.

The fish willinglychose test fieldswith green and bluesurrounds,but they were much less cooperativewith redand yellow surrounds. Consequently, we could notcollect as many choices with the red surround as withthe other colored surrounds. With the yellow surround,however, we used an artifice to increase the number ofchoices: in some sessionswe added a black star of aboutthe same size as the test fieldsand fed the fishat it. In thisway, we could “lure” the fish to swim to the yellow diskwith the test fields and bite at them.

SIMULTANEOUSCOLORCONTRASTIN GOLDFISH 1585

(a) Y

A

(b) Y

660-750x z

FIGURE4. Colorloci of test fields in goldfishcolor space. The trianglerepresents the base of the tetrahedron (the contributionof the uv-conetype is not taken into account).x,y, z: relative absorptionof S-, M-, andL-cone type of goldfish.460-750: loci of spectral colors. (a) Loci ofthe colorsused in Experiment1. V, color loci of the test fields(G3–G1,T, R1–R6).~, trainingfieldT; 0, color loci of surrounds(green, red);., gray trainingsurround.(b) Loci of the colors used in Experiment2.V, color loci of the test fields (B6-B1, T, Y1-Y8); ~, trainingfieldT;

0, loci of surrounds(blue, yellow); ●, training surround.

Data

The number of choices per experiment depended onhunger and motivation of the goldfish.The data for thetraining surrounds were collected during the “trainingsessions” at the beginning of the experiments. “Testsessions” gave 40–80 choices per day. In Experiment 2each experiment consisted of 60 choices. The choicesobtained in different experimentswith the same surroundcolor on different dayschoice frequencies (incalculated. Each fishstrategy”, and thereforeseparately. We plotted

were pooled, and the relativepercent) for each test fieldshowed a different “choicewe plotted the individual datathe relative choice frequency

against the test fields, as characterized by their colornames in the diagrams.

Calculation of “goldfish-specijic” chromaticities (colormetrics)

The test fieldcolorsunder the illuminationsused in theexperiment were specified in terms of chromaticitycoordinates of goldfish color space, in the same way asdescribed by Neumeyer (1980) for the honeybee. Thecalculation of color space is based on the absorptionspectra of the four goldfish cone photopigments mea-sured microspectrophotometrically (Bowmaker et al.,1991). The effect of the spectral distribution of lightreflectedby the papers used as test fieldsor surroundsoneach photoreceptorwas calculated as follows:

s

750w= aUv(A)~(A)#(A)dA,

300

I

750x= aX(A)~(A)#(A) d~,

300

[

750Y= ay(~)~(~)~(~) d~,

300

~

750z= az(A)f?(~)@(A)dA

300

with a(l) referring to the relative spectral absorption ofthe cone type (ZW:UV-cone,x: S-cone,y: M-cone, z: L-Leone),P(2) the relative spectral reflectanceof paper and~(~) the spectral distribution of the illuminating lightcorrected for quantal energy.

The relative absorption of each photoreceptor wascalculated according to:

Uv“ uv/uv + x + Y + z,x = x/uv + x ‘+ Y + z,

Y = y/uv +x + Y + z,z = z/lJv +x +-Y+ z “’ ““““1:2’

These valuescan be plotted as“co@dinatesof a Mint in,,a tetrahedron. ,Each point, the so-called’,“col’brlocus”,represents the relative excitation ~alues of the four conetypes caused by a color stimulus. B does not containinformation about absolute excitation. The illuminationused in the experimentsemitted almostno light in the UVrange. Thus, the UV-cone was excited only slightly bythe test fields. Therefore, we neglected the “thirddimension”of the color space and plotted the color lociin the goldfishcolor triangle that represents the relativeexcitation of the S-, M-, and L-cone. Figure 4(a) showsthe color loci of red–green test fields and surroundsusedin Experiment 1 together with the loci of the spectralcolors in the color triangle. In Fig. 4(b) the color loci ofblue–yellowtest fieldsand surroundsof Experiment2 areplotted.

“Goldfish-specific”brightnessThe relative brightness B of test field and surround

papers was estimated by using the spectral sensitivityfunction of goldfish measured in training experiments

1586 S. DORR AND C. NEUMEYER

~ 0.8m i IE~ 0.6&$ 0.4.-32 0.2

0G3 G2 G1 T RI R2 R3 R4R5 R6greredIgrygry

test fields

I“,

al

~ 0.6.-;~ 0.4.-5z 0.2

0B6 B5 B4B3B2B1 T Y1 Y2 Y3 Y4 Y5 Y6 V Y8yelblublc

test fields

FIGURE 5. Goldfish-specificbrightness of test fields and surroundsrelated to the value of magnesium oxide = 1. (a) Test field andsurround colors used in Experiment 1, illuminated by the fluorescenttubes (Fig. 3). G3–R6:test fields; gre: green, red: red, lgry: light graytest surround, and gry: gray training surround. (b) Test field andsurround colors used in Experiment 2, illuminated by the white lightshownin Fig. 3 (continuousline). B6-Y8: test fields; yel: yellow,blu:

blue test surround,and blc: black training surround.

(Neumeyer, 1984). The calculation was performedaccording to:

~

720B= S(A),6(A)@(A)d~

400

with S(l) referring to the behaviorallymeasured spectralsensitivity,~(l) the relative spectral reflectanceof paperand ~(l) the spectraldistributionof the illuminatinglightcorrected for quantal energy. The integration interval islimited by the range over which the spectral sensitivityfunction was measured. The relative goldfish specificbrightness B was normalized relative to that of magne-sium oxide for the illumination in question. Figure 5(a)shows the brightnessof test fields and surroundsused inExperiment 1, Fig. 5(b) that of those used in Experiment2.

RESULTS

Effect of differently colored surrounds

Goldfish trained on an orange training field with graysurround were tested with a green and red surround

(Experiment 1). Goldfish trained on a bluish-graytraining field with black surround were tested with ablue and yellow surround(Experiment2). The surroundscovered the entire disk.

Experiment 1. In the training situation with graysurround each of the three fish chose the orange trainingfield Tin about 80% of cases as shown in Fig. 6 (blacksymbols).Fish K. also chose similar test fieldsR1 and R2with a frequency of about 10%. (These test fields werenot presented to fish S. and M.) In the test situationwithgreen surround, the choice behavior changed. Thegoldfish chose the training field in less than 10% ofcases (Fig. 6, hatchedbars). Instead,all of them preferreda yellow test field, G1. Fish M. and S. chose it as often asthe trainingfieldwith the gray surround[Fig.6(a, b)], fishK. in only 40% of cases [Fig. 6(c)]. This fish also“pecked” additionally at an orange test field (Rl) and ayellow–greentest field (G3) in about 20% of cases each.

With a red surround, the three fish preferred red testfieldsinsteadof the trainingfield.Fish M. and S. selecteda red test field, R4, with a frequency of 60% and alsochoseother red test fields [Fig.6(d, e)]. Fish M. chose thetraining field only in 1% of cases, but fish S. in about20%. The relative choice frequency of fish K. on thetraining field dropped to 5!Z0.Instead it chose the red testfields R2 and R4 with a frequency of about 25% each[Fig. 6(f)].

Experiment 2. Fish C. chose the bluish–gray trainingfield in about 35% of cases in the training situation withblack surround.It also selected similar test fields Bl, B2and G1 in 15–205Z0of cases [Fig. 7(a), filled symbols].Fish G. chose the training fieId in about 45% of cases.Test fieldsB1 and Yl, closest in hue to the training field,were not presented to this fish. It chose test field Y3 witha frequencyof 15Y0,which is clearly more often than fishC. [Fig. 7(b), filled symbols]. Note that nevertheless the“width” of the choice distribution is the same for bothanimals.

When the surroundwas changed to blue, both fish didnot choose the training field any more but decided formore bluish test fields. Fish C. chose the two blue testfieldsB4 and B6 in about 25% of cases, followed by testfield B3 in about 15% of cases [Fig. 7(a), hatched bars].Fish G. “pecked”most often at the blue test fieldB3 witha frequency of 409Z0[Fig. 7(b), hatched bars].

In the test situation with yellow surround the relativechoice frequency of both fish on the training fielddroppedto 10%.Both fishchoseyellowtest fieldsinsteadbut with no clear preference [Fig. 7(c, d)].

In each of the four test situationsthe goldfishchangedtheir choice behavior. They did not choose their trainingfield but one of the other test fields. With this choicebehavior they indicate the test field that most closelyresembles the training field in the training situation.Thechoices of the goldfishare always in the direction of thehue of the surround, consistent with a compensation ofthe induced hue shift away from the surround, the effectof simultaneouscolor contrast.

SIMULTANEOUSCOLOR CONTRASTIN GOLDFISH 1587

(a)

fish M.

/\

green

gray

G3 G2 GI 1 RI R2 R3 R4 R5 R6

test fields

l’\ green

gray~

“ .~

d3 G2 G1 i i R2 R3 R4 R5 R6

test fields

(c)

fish K,

green

gray~

G3 G2 G1 T R1 R2 R3 R4 R5 R6

test fields

fish M.

red

gray~

G3 G2 G1 T R1 R2 R3 R4 R5 R6

test fields

(e)~ 100 ~.

“g 40c0

red

~

1 IG3 G2 G1 T R1 R2 R3 R4 R5 R6

test fields

(f)

fishK.

red

gray:A

G3 G2 G1 T R1 R2 R3 R4 R5 R6

test fields

FIGURE 6. Choice distributions with green (a-c) and red (d–~ surrounds (Experiment 1). Abscissa: test field notations;ordinate: relative choice frequencyin percent. Filled symbols:training result with gray surround.(a) and (d) Results offish M.(Test fields RI and R2 were not presented to this fish. However,they are plotted on the abscissa for better comparisonwith thechoice distributionof fish K.) (b) and (e) Results of fish S. (test fields RI and R2 were not presented). (c) and (f) Results of fishK. Number of choices in the training situationswith gray surround:between 1643and 2648; in the tests with green surround:

between 216 and 361, with red surround:between 19 (S.) and 123(K.).

Effect of brightnesscontrast contrast. To show the effect of brightness contrast we

The colored test fieldsdifferedfor the goldfishnot only tested fish K. with a light gray surround. If brightnessin hue but also in brightness (Fig. 5), especially in contrast is induced by a brighter surround all test fieldsExperiment 1. All colored test surrounds were brighter shouldlook darker to the goldfish.Therefore, they shouldthan the training surround. Therefore, it is possible that choose a test field brighter than the training field (forthe change of choice behavior with colored surrounds is example, test fields G3–G1, Rl, R2) to compensate fornot only due to color contrast but also to brightness this change. As shown in Fig. 8, fish K. chose the orange

S. DORR AND C. NEUMEYER

)

fish C.

A blue

B6 B5 84 B3 B2 B1 T Y1 Y2 Y3 Y4 Y5 Y6 W Y8test fields

(b)

test fields

(c)~500

$40aaS30=al

“g 20co,: 10~go

B6 B5 B4 B3 B2 B1 T Y1 Y2 Y3 Y4 Y5 Y6 Y7 Y8test fields

(d)

B6 B5 B4 B3 B2 B1 T Y1 Y2 Y3 Y4 Y5 Y6 V Y8

test fields

FIGURE7. Choice distributionswith blue (a and b) and yellow (c and d) surrounds(Experiment2). Filled symbols: trainingresult with black surround.(a) and (c) Resultsof fish C. (b) and (d) Resultsof fish G. (Test fieldsB1 and Y1 were not presentedto fish G.). Number of choices in the training situations with black surround:2810 (C.) and 720 (G.); in the tests with blue

surround: 180;with yellow surround: 120.

test fieldsRI and R2 slightIymore often in the test than inthe trainingsituation.But this choicedistributionis by nomeans comparable to that with greenand red surrounds.Thus, there is a genuine effect of the colored surroundsbased on color contrast.

Effect of surroundsize

If simultaneous color contrast is due to lateralinteractions across neighboring areas in the retina, arelatively small annular surround should elicit a colorcontrast comparableto that of a full surround.Therefore,we reduced the surround to narrow annuli of varyingwidth. The remaining area on the disk was covered withthe gray training surround. (This experiment wasperformed with test field and surround colors ofExperiment 1 only.) Figure 9(a) shows the relativechoice distributionof fish M. on all test fields with fourdifferent annulus widths of the green surround (outerdiameters: 4.5, 3.7, 3.0, and 2.5 cm; inner diameter:2.2 cm), and a constant test field size of 2.2 cm diameter.The diagram shows that only the results for trainingfieldT and yellow test fieldG1 varied, the choiceson the othertest fields remained unaffected. Therefore, it is reason-able to plot the values for trainingfieldT and test fieldG1

only,for a clear presentation,withoutloss of information.In Fig. 9(b) the results are plotted as a function ofsurroundwidth. The relative choice frequency values ofall three fishare similar.Comparisonwith the distributionin the training situation [“0 cm (green) surroundwidth”]shows that the choiceson trainingfieldT [Fig.9(b), opensymbols] decreased with increasing ~idth of the green

a)v.-2v

80

60

40

20

0G3 G2 G1 T RI R2 R3 R4 R5 R6

test fields

FIGURE 8. Choice distribution of fish K. in a test with light graysurruund.Filled symbols:training result with gray surround.Test fielddiameter: 0.4 cm [see Fig. 9(a) for comparison]. Number of choices:

training, n = 794; test, n = 119.

SIMULTANEOUSCOLOR

surround, while those on yellow test field G1 [Fig. 9(b),solid symbols] increased. The effect of the large greensurround that covered the entire disk is also plotted. Theresults show that simultaneouscolor contrast intensifieswith surround width, but that the effect does not further

fish M.

-! ❑ 1,15N 0,75❑ 0,4

G3 G2 G1 T RI R2 R3 R4 R5 R6

test fields

(b)

0 1 2 1.s.

surround width [cm]

(c)

a)0.-

2u

80-

60-

40-

20-

LA

@2,5

0-0 1 2 1.s.

surround width [cm]

0.2 0.4 0.6 0.8 1 1.2test field radius [Cm]

CONTRASTIN GOLDFISH 1589

increase beyond surround widths of 1.2 cm. It isremarkable that even the smallest surround of 0.15 cmwidth had an effect on the choice behavior of the fish.Assuming a viewing distance of 5 cm, this surroundwidth correspondsto a visual angle of 1.7 deg, with thetest field subtending25 deg.

In a subsequentexperiment the outer diameter of thissmallest green annulus was kept constant (2.5 cm)whereas the diameter of the test fields was reduced.Each fishchosetrainingfieldT less and test fieldG1 moreoften with decreasingtest field size, and, thus, increasingsurround width [Fig. 9(c)]. It seemed possible that thiswas an artefact due to the smaller test field sizes. Weexcluded this possibilityby training the goldfishon suchsmall test fieldswith gray training surrounds.In each ofthese trainingsituationsthe fishchose the trainingfield ingeneral as often as with the original test field diameter of2.2 cm and they did not “peck” at yellow test field G1[Fig. 9(d)].

The choices on training field T of each fish for thesetwo experimentswere replotted as a function of the ratioof surround width and test field radius (Fig. 10). Theresults of the three fish showed only small differencessothat all data points could be fitted by one exponentialfunction. This indicates that simultaneouscolor contrastdoes not depend on the absolute size of test field andsurroundbut only on the size relative to each other.

DISCUSSION

Direction and strength of simultaneouscolor contrast

With each of the four tested colored surroundsgoldfishchangedtheir choicebehaviorand “matched”the trainingfieldwith gray (or black) surroundwith one of the othertest tklds: they chose a “greener” test field with greensurround,a “redder”one with red surround,a “bluer”onewith blue surround and “yellower” ones with yellowsurround. Direction and strength of simultaneous colorcontrast can be inferred from the presentationof the testfield and surround colors in goldfishcolor space. In Fig.n(a), the situationfor Experiment 1 is shown. Here, thefish changed their choice behavior and preferred yellowtest field G1 instead of the training field T when the testfieldswere presentedwith a green surround.This change

FIGURE9. Choicebehaviorwithvariable surroundwidthandtest fielddiameters. (a) Choice distribution of fish M. with green annularsurroundbetween Ocm (gray training surround)and 1.12cm widths.Test field diameter: 2.2 cm. (b) Effect of green annular surroundas afunction of surroundwidth [data from (a)]. The diameter of the testfields was constant (2.2 cm). Surround width O: result with graytraining surround. 1.s.:large green surround covering the entire disk(23 cm diameter). Ordinate: relative choice frequencyvalues of threegoldfishat trainingfieldT and at test fieldG1 only.Fish M.: T: ❑, Gl:■; fish S.: T: *, Gl: A; fish K.: T: 0, Gl: ●. (c) Effect of greenannularsurroundof constantouter diameter (2.5 cm) with test fieldsofvariableradii.ChoicefrequenciesofthreegoldfishattrainingfieldTandtest fieldG1.1.s.:large green surroundcoveringthe entire disk (testfieldradius0.2 cm). (d) Choiceson the trainingfieldT andtest fieldG1with large gray training surroundand test fields of various small radii

(control experiment).

1590 S. DORR AND C. NEUMEYER

(a)

8

, ,XJy = 67*exp(-1.5 x)+ 9

.

40 -“

. 00 *

o ●

O 2 4 6 8 10 “ 56.5surround width/test field radius

FIGURE 10. Choices of three goldfishon the training field T plottedagainst the ratio of surround width and test field radius. Data pointsshown in Fig. 9 are fitted by eye by one exponentialfunction. For thesurround covering the entire disk a surround radius of 11.5cm wasassumed for each test field, leading to a ratio of 9.45 (11.5–1.1)/1.1

and 56.5 (11.5–0.2)/0.2.

(b)

in choice behavior is indicatedby the solid arrow. As thefishhad learned to select the hue of the trainingfield,theirchoice of the yellow test field G1 in the test situationmeans that, with the green surround, it appeared like theorange training field T with the gray surround. Thus, itcan be concluded that the hue of all test fieldsare shiftedtowards “redder” (or “less green”)by the green surround.The fish choose a “greener” test field to compensate forthis hue shift. It is the yellow test field G1 that resemblesthe trained hue best. The dotted arrow in Fig. n(a)symbolizes the strength and direction of color contrast.

With a red surroundthe fish preferred the red test fieldR4. The change in choicebehaviorfrom the trainingfieldT with gray surround to red test field R4 is also indicatedby a solid arrow in Fig. n(a). The inferred hue shift dueto the red surround is representedby the dotted arrow.

A similar graph for Experiment 2 is shown in Fig.n(b). Fish C. preferred test fields B4 and B6 with theblue surround.Fish G. preferred test field B3. The choicebehavior of both fish is represented by the solid arrowpointing from T to test field B4. In “thetest with theyellow surround the results were not s~ clear..Both fishpreferred yellow test fields, although they aIso occasion-ally chose blue test fields.They opted slightlymore oftenfor test field Y8 which is marked in Fig. Ii(b). Thebroadly scattered choice distribution can have severalexplanations. Possibly the fish could not decide on onetest fieldbecause,with the yellowsurround,noneof themresembled the trained hue. Furthermore, the fish couldhave been bewildered by the yellow surround. Asdescribed in “Materials and Methods”, the fish did notswim to the test fields with the yellow surround at thebeginning. Only after an intermediate training (beingrewarded on a black star) did the fish make choices.

The graphs show that goldfish choose test field huestowards the surroundingcolor (solid arrows in Fig. 11).From this compensatory“colormatch” of the goldfishweinferred that simultaneouscolor contrast changes the testfield hues “away” from the surrounding color (dottedarrows in Fig. 11). Of course, it is possible that the

gray

\●

green

\Q\

fGI

T

q-

\.,,vv..,

‘“v IU

red—-Jo

/

FIGURE 11. Color contrast effect of the colored surroundsshown inthe color triangle (“z’’-cornerfrom Fig. 4). (a) Results of Experiment 1(from Fig. 6); (b) results of Experiment 2 (from Fig. 7). The solidarrows indicate the shift of choice behavior from the training situationwith gray (a) or black (b) surroundto the test situations with coloredsurrounds.The contrast effect of colored surround, i.e., the change inhue of the test fields is shownby the dotted arrows(from G1 and R4 toTin (a), andfrom B4 andY8to T in (b). Dottedarrowsof the same sizeand directioncan in fact be drawnat each test field locus. V, color lociof test fields; ~, loci of training fields; 0, loci of training surrounds;

●, colored surrounds.

direction of the induced hue shift does not coincidewiththe direction of the axis connecting the test field lociwithin the color space. Then, the color contrast effectwould not be entirely reflectedby the choice behavior ofthe fish. In such a case, we expect the goldfishto choosethe most similar test field and to “project” the inducedhue onto the “color axis” of the test fields. This wasprobably the case with the green surround in Experiment1. Here, the line connecting the color loci of the graytraining surround and the green surround is not in thesame direction in the color space as the loci of the testfields. The green surround excited the short wavelengthcone type less than the gray surround, and the middlewavelengthcone type only slightlymore. Therefore, onewould expect only a very small hue shift towards “more

SIMULTANEOUSCOLOR CONTRASTIN GOLDFISH 1591

red” inducedby the green surround.The observedshift inchoice behavior from T towards the adjacent, moreyellow test field G1 was indeed small, but neverthelessvery clear.

The degree of the color contrast effect can be inferredfrom the test fieldschosen: a choice of a neighboringtestfield indicates a weaker contrast effect than the choice ofa test field near the border of the set. Thus, the arrows inFig. 11 give a hint of the strength of color contrast.However, it is not possible to compare the effects ofdifferentlycolored surrounds.As the metrics “inside”thecolor space of goldfish are unknown, the distancesbetween two loci are not defined. In other words, we donot know how similaror dissimilartwo colorslocated at aparticular distance from each other in color space appearto the goldfish. This is known only for spectral colors(Neumeyer, 1986;Fratzer et al., 1994).

Effect of brightnesscontrastAs all surround colors were brighter than the training

surrounds, and in Experiment 1 the test fields were notadjusted to equal brightness (Fig. 5), it seemed possiblethat brightness contrast may have influencedthe results.Therefore, we tested the effect of a light gray surround,i.e., a surround of the same hue as the training surroundbut of higherbrightness.If brightnesscontrastin this caseleads to a darker appearanceof test fields (as in humans),goldfish should choose a test field with the same hue asthe training field but with a higher brightness tocompensate for this effect. As such a test field did notexist in the sample, the fish shouldmake a “compromise”and choosea test fieldmost similar to the trainedhue, andadditionallyslightlybrighter.The minorchange in choicebehavior with slightly higher frequencies on R1 and R2mightbe interpretedin this respect (Fig. 8). However,testfield G1 was also brighter, but was never chosen.Furthermore, the shift with red surroundwas in the samedirection as the minor effect of the light gray surround.However, test field R4, the one preferred with the redsurround,was darker than the trainingfield.Therefore, itis very unlikely that brightness contrast, which wasshownby Herter (1930) in teleost fishes,had an influenceon the choice behavior with red and green surrounds.

Effect of spatial stimulus configurationon color contrast

Simultaneous color contrast decreased with reducedsize of the green surround. However, with an annuluswidth of 1.15 cm and a test field radius of 1.1 cm colorcontrastwas as high as with a large colored surroundthatcovered the entire disk [Fig. 9(b)]. Thus, the strength ofsimultaneous color contrast depends on the size of thecolored surroundin a small range only.When we kept theouter diameter of the surround constantly small andreduced the test field diameter, simultaneous colorcontrast increased [Fig. 9(c)]. The data of both experi-ments plotted against the ratio: surround width/test fieldradius could be described by a common power functionfor all three goldfish.The curve becomes flat at about aratio of 1:1, indicating that maximal color contrast is

already gained when the annulus is as wide as the radiusof the test field (Fig. 10).This holds true within the testedlimits of test field sizes. Assuming the smallest possibleviewing distance of 3 cm, the test fields covered a visualangle of 7.6-40.3 deg, and annulus widths varied from2.9 to 21 deg.

Simultaneous color contrast is dependent on spatialconfiguration of the stimulus and surround in humansalso (Kirschmann, 1891; Jameson & Hurvich, 1961;Heinrich, 1967; Walraven, 1973; Walraven, 1976;Valberg, 1974; Tiplitz BlackWell& Buchsbaum, 1988).Heinrich (1967)showed that a surroundlarger than 5 degdoes not increase simultaneouscolor contrast induced ona 2.5 deg x 2.5 deg test field. Walraven (1973) measuredalmost maximal color induction with 150 min of arcsurround diameter on a test stimulus with 90 min of arcdiameter. Valberg (1974) found maximal inductionwitha 6 deg x 6 deg surround on a test field with 2 degdiameter. Tiplitz BlackWell & Buchsbaum (1988)observed maximal color contrast induced on a0.62 deg x 0.62 deg test field by a surround with 20 minof arc width. Brenner et al. (1989) claimed simultaneouscolor contrast to be strongestwith 1 deg surround widthand a test stimulus of 0.75 deg x 0.75 deg. Very smallsurroundwidths of 33 min of arc were also sufficient toperceive a field subtending 2.2 deg as a surface colorrather than as a self illuminant (Uchikawa et al., 1989).These studies, carried out with most diverse methods,revealed ratios of surroundwidth/test field radius (in theway we calculated them for our data) of between 0.6:1and 2.6:1. Thus, the ratio of 1:1 we obtained for goldfishfalls within this range.

In the honeybee,color contrastdid not further increasewith surrounds of 5–10 mm for test fields of 10 mmdiameter (Neumeyer, 1980). The honeybee data werereplotted against inducing area/test area by Varela et al.(1993)and compared to results in pigeons (Budnik, 1985cited according to Varela et al., 1993).The responses ofthe two species dependent on geometrical parametersseem to be equal and maximal contrast induction wasreached at abouta 1:1ratio, the same ratio as we obtainedfor goldfish.

Our data suggest that simultaneous color contrast ingoldfishdoesnot dependon the absolutestimulussize (inthe tested range) but only on the ratio between surroundsize and test field size. To our knowledge, this relation-ship has not been investigated explicitly in honeybees,pigeons,and humans,but was theoreticallydemandedforhumansby Jameson & Hurvich (1964). Our data fitted anexponentialfunction.The relation of simultaneouscolorcontrast to the surround size is best described byexponential functions in humans also (Valberg, 1974;Walraven, 1973;Tiplitz Blackwell& Buchsbaum,1988).

Possiblephysiological basis and biological significanceof color contrast

As the goldfishwas moving freely in the experimentsdescribed, it was not possible to present test field andsurround in such a way that they stimulated adjacent

1592 S. DORR AND C, NEUMEYER

areas in the retina strictly simultaneously.Even with thesmallestsurroundit is possiblethat the area stimulatedbythe test fieldhad been stimulatedby the colored surroundimmediately before. Therefore, it is possible thatsuccessive color contrast was involved as an aftereffectof chromatic adaptation. In principle, successive colorcontrast can be shown with the same method assimultaneouscolor contrast: here, the animal is exposedto a large coloredfield(samecolor as used for surroundinthe simultaneous color contrast experiment) for severalminutes.Then, the large coloredfield is removed,and thetest fields are presented on a gray surround immediatelyafterwards. With an aftereffect of chromatic adaptation,the choicebehaviorchangesto other test fieldsindicatingchanges in perceived test field hues. With this method itwas shown in the honeybee that exposure to a coloredfield for 5 min yields an aftereffectwhich lasts for about3 min (Neumeyer, 1981). In the goldfish, however, wecould not find any indicationof successivecolor contrasteven after 15 min of adaptationto a coloredfield.We alsodid not find an aftereffect of chromatic adaptationin ourcolor constancyexperimentsafter prolongedpresentationof the colored illumination (Dorr and Fritsch, unpub-lished results), a condition under which the honeybeesshowed strong effects (Neumeyer, 1981).

Bearing this in mind there are two possible explana-tions of the simultaneouscolor contrast effects we wereable to measure: (1) lateral neural interactionsbetweenneighboringareas stimulatedsimultaneouslyby test fieldand surround; and (2) effects of very fast chromaticadaptation.

Lateral interactions could cause color contrast in twodifferent ways: either by mutual excitation of cone“channels”with different spectral input, or by inhibitionbetween cone “channels” with the same spectral input(Cornsweet, 1970; Creutzfeldt et al., 1990). The latterpossibility is realized in the double-opponentganglionand bipolar cells of goldfishcharacterizedelectrophysio-Iogically by Daw (1967, 1968) (see also Daw, 1984 andKaneko & Tachibana, 1981).These cells are excited forexample by “red” in the center and inhibitedby “red” inthe surround, at the same time they are inhibited by“green” in the center and excited by “red” in thesurround. Such a cell is optimally excited by a greentest field surroundedby red, but also to some extentwhenthe test field is gray and surroundedby red.

Lateral inhibition between “cone channels” of thesame spectral type would lead to a decreaseof excitationin the neighborhood.In the case of a gray test fieldwithina red surround, the long wavelength cones stronglystimulated by the surround will selectively inhibit thelong wavelength cones stimulated by the adjacent testfield.This shouldcause a changeof the excitationratio ofthe cone types, and thus a shift in perceived hue towardsthe complementarycolor.

The change of excitation ratio caused by this type oflateral inhibition is the same as the effect of sensitivityreductionby selectivechromaticadaptationwhich can bedescribed by the von Kries coefficient law (von K.ries,

1905;Wyszecki & Stiles, 1982). If chromatic adaptationto narrow annular surrounds accounts for simultaneouscolorcontrastin our experiments,then we have to assumethat adaptation is a very fast process with a shortaftereffect. The time course of adaptation in ganglioncells was measured in primates recently (Yeh et al.,1996). Correspondingexperiments are required in gold-fish. More detailed studies of the spatial properties ofretinal ganglion cells are also necessary. Electrophysio-logical measurements revealed many chromatic typeswith complicated receptive field structures (e.g. Spek-reijse et al., 1972;van Dijk, 1985).Further investigationswould also be important for our understandingof coIorconstancy, an ability well developed in goldfish colorvision (Ingle, 1985; Dorr, 1996; Dorr & Neumeyer,1996), in which the same neural mechanisms may beinvolved.

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Acknowledgements—We would like to thank Dr. J. Schramme forsolving all kinds of computer problems and M. Grosz, W. Hoch, H.Huber and J. Aftmayer for technical help. We are grateful to NeilBeckhaus for improving the English. The project was supported byDeutscheForschungsgemeinschaft(Ne 215/9)and the HumanFrontierScience Program (H. Spekreijse).