Spatial and chromatic antagonism between the long- and middle-wavelength cones in the detection of long-wavelength flashes

RESEARCH NOTE SPATIAL AND CHROMATIC ANTAGONISM BETWEEN THE LONG- AND Mr~~L~-WAVELENGTH CONES IN THE ~ETE~T~~N OF LONG~AV~L~N~TH FLASHES YOSH~MICPI~ EJIMA’

and SHICEKO TAKAHAW?

‘Department of Psychology, The College of Liberal Arts, Kyoto University, Yoshidanihonmatsu-cRo, Sakyo-ku. Kyoto 606, Japan and 2Department of Psychology, Faculty of Letters, Kyoto University, Ynshidahonmachi, Sakyo-ku, Kyoto 606, Japan

Abstract-Field ddditivity was tested for small red increments on small and large adapting fields. The results for a large adapting field showed the faifure of field addi~ivity of the canceiialion type, providing strong evidence for come-antagonistic coding, wkiie the results for a small adapting field skewed field add~~~v~~y~ The ~d~~~~]a~iO~ elect took place ~~c~rre~~ly with tke spatial sens~~~za~io~e&X, thus suggesting that the spatial and chromatic antagonism occur cnncomjt~ntiy at some stage in the detection pathway. Spatial antagonism

Receptive field

Color-opponency

In recent years, a number of investigators have ~~arnin~d the additive property of the 3ts mechanism to assess the degree to WhiCh knoWfl photoreceptor prqxtties &ZZfl account for the behavior of the mechanism. FaiIures of arid-additjv~ty tead to the view that adaptation occurs not only in receptor site but also centraI to the receptors where signals are pooled at a past-receptoral

site.

The occurrence of test- and ~eld~additivjty failures depends on the stimulus parameters. The test-additiviry results of Boynton et ai. i I9641 and Stifes (1957, 1978) show that short duration gashes are approximat~Iy test additive, while long duration flashes fail to be test additive. Wandefl and Pugh f 198&s, b) observed field addjtivity with short duration flashes but !ieIds were subadditive for long duration flashes. The intensity of the field strongly influenced the subadditive effect. Marked subadditivity was observed with high tieId intensity and the subaddjtivity was reduced at low field intensities (Wandell and Pugh, 198Ob: Strameyer et al., f98S). The failures of the test- and fieldadditivity can be explained by positing inreractions among the ~h~t~recept~rs ~~o~~t~~

and Baron, 1982; Wandell and Pugh, 19%&a,b; Wandell et al., 1982a, b; Stromeyer et af., 198.5). Reeves (1981) found that transient desensitization occurred after extinction red and green backgrounds but the threshold felf if the background was yellow, or if the red or green background was sIowty Aickered during adaptation, or if the test was small and brief. His finding also suggests cone-antagonistic adaptation. The present study considers how spatial parameters affect the detection threshold. It is well known that sensitivity is strongly controlled by lateral spatial interactions (Crawford, 1940; Barlow, 1957; Buss ef al., 1982). Ph~s~o~~~~caI~~, the majority of the foveal c&s show cenrersurround urgan~ation with M and t cone opponency: one class of cones forms an excitatory or inhibitory center and the other class forms a wider antagonistic area that may overlap the center and produces a surround (Gouras and Zrenner, 1981). However, there is little psychophysical evidence for color-opponent interactions in the center-surround mechanisms McKee and Westheimer (1970) measured the fovea1 Westheimer function, which presumably reflects retinal events (Enoch rf aI., 197&_fohnson and Enoch, 19761, using the two-color

hxarch

Note

that in the

image

1996

threshold central

technique. fovea

anisms”

suggesting

cone

lateral port

class.

that

mediated do not

of

always

of center-surround

1973;

Stromeyer

198 1, Stromeyer, this

tudy,

we

field-mixture varying

field size. We found

cone-antagonistic

surround

spatial

in

organization.

to optimize

conditions

antagonistic

pathways.

the

strong evidence

coding

test flash and high-field

Foster,

et al., 1985).

experiments,

the

center-

were employed

for detection

and interference

by cone-

Thresholds After

test was just visible. a block

ground

was always were used veiling

of a test

concentric

field whose diameter

the range 5-40’.

back-

was altered

The wavelength

630 nm. Lights

within

of the test spot

of 530 and 650 nm

for the background field. An auxiliary of dia 10” (650 nm) masked

background

stray light. mark. view

consisted

a steady

A set of tiny dots served as a fixation

The stimuli through

were presented

a 2-mm-dia

test spot was presented Stimuli

were produced

in Maxwellian

artificial

with with

pupil.

The

2OOmsec duration.

a five-channel Max-

we&an

view

optical

system

with

three

light

sources

(a

500 W

xenon

arc

and

two

halogen-tungsten

lamps).

the 3’ test target,

two

ground

field,

veiling

and

the

One

formed

handwidth.

The

was controlled intensity density Head

intensity

with and

alignment

bite on a X---Y-Z

the

All beams were

with grating monofilters of 5-6 nm half of

neutral

the

background

density

of the test was controlled filters

back-

two formed

marks.

rendered monochromatic chromators or interference

provided

the small

other

field and fixation

beam

varying

the

was maintained

filters.

The

reversal

voltage.

with

a dental

manipulator.

radiant

fluxes

of

beams were measured

the

by an audible

tone

and followed

by ;I

one interval

the interval

the test.

three-times

of the test

was

and the test was incremented

after was

0.07 log units, and ailcr ;I first

half

to

The mean of the first six peaks and

in the resulting

the estimate threshold

sequence

of the light 1965).

Each

At least four out.

First,

W;LS taken

intensity

of 0.79 probability

Levitt,

carried

con-

light

was made, all steps were reduced

valleys

con-

observer

containing

was right

intensity

The

The step size in the decrement

this value.

trials.

was then given

(200 msec).

the observer

for

so the

Each trial consis-

tone. Only

the test spot

first set to about

that

correct run

a

(Wetherill

required

runs per datum we measured

as

yields

30-50

point threshold

were vs

intensity curves for background fields of 530 and 650 nm. Field additivity was then tested. The intensity

of the 650~nm field was fixed,

the intensity

of

increasing

Field

the small

by a scattered minance

530~nm

backgrounds

To avoid veiling

the

amounts.

sured with

light,

field

additivity

of the small

WL~S

and in mca-

of 5’ and 40’ dia. test from

the intensity

background

admixed

was

set to

being

detected

of the large red l/50

red background.

the

iilu-

The veil

slightly lowered threshold (~5%). but it had little influence on the shape of the threshold vs intensity

curve

(for

40’ licld).

Authors served as observers. They were both within the limits of normal trichromatic color vision

The

marked

by 500msec.

response-feedback

and

trials.

field

point

by neutral

lamp

Calibration

light

The observer

ted of two intervals

the

;I tcmpor;tI.

set the starting

of self-initiated

tained

with

staircase.

to the background

the observer

decremented,

configuration

density

calibrated

(Hitachi).

forced-choice

adapting

2 min,

each error.

3’ and

were cali-

lamp. The neutral

were measured

two-alternative

secutively,

Apparartts

of dia

Westheimer’s

filters were spectrally

had to choose

METHOD

The stimulus

Retinal

a photoelectric

using

a spectrophotometer

When

spot

(Toshiba),

and separated

A long-duration

intensity

with

(1966). The monochromators with a mercury

with

radiometer.

for 1973:

1978;

performed

increment-threshold background

et ul.,

EG&G

intcr-

(Bender.

1983; Stromeyer

an

was measured

sup-

spatial

interaction

method brated

by a sin-

investigations

with

illuminance illuminometer

each mech-

but they fail to show clear evidence

Kelly,

for

mech-

is cone-selective

Subsequent

color-opponent

In

within

there

interactions

this view

color

in that desensitizing

antagonism

spatial

actions,

green

zones existed

center-surround gle

red and

were independent

and sensitizing anism,

They concluded

“the

monochromatic

at the Maxwellian

according to tests with a Nagel anomathe Ishihara pseudoisochromatic loscope, plates, and the Farnsworth MLIINC~I IOO-huc test.

Note

Research

I997

_____.-___ _..____--

,L, , , ,a,a,; 5

6

field

Log Fig,

1. A field-mixture

of 40’

and

thresholds

target

is the

prediction

chromatic (open

with

was

curves

of field-additivity. are

the

for

The

open

upon

fields

200 msec

for

tlash.

diameter

are the thresholds

of 5’. The

thresholds

530nm

the field

squares)

field for the field diameter

squares)

and

3’. and

field

(solid

I10

b l’o1:

field intensity

(rrz:530nm

1

quanta(~,:650nm)deg-‘sec~’

650

630 nm,

the monochromatic

the increment-threshold

9

0

intensity

experiment

5’. A test upon

7

; P

Log

circles points

the

field

Y.E..

represent

of 40’.

The

points

intervening

the field mixtures.

between

The

the licld

circles

increment

intervening

for

solid

upon

represent

mixtures.

observer The

upon

the

the increment-threshold curve

between

The broken

thresholds

intermittent

diamctcr increment

is the

curve monocurves

prediction

of

field-additivity.

Results

left curve shows data for the 650-nm field, and the right curve shows data for the 530-nm field. Each set of data (within 1.44 log unit of threshold upon the auxiliary field alone) was fitted by the Stiles template (Wyszecki and Stiles, 1982). The data coincide with the template except for the high intensity thresholds for the 530-nm field, which fall below the template. The intervening points denoted by solid squares were obtained in the field-mixture ex-

Figures 1 and 2 show for the two observers the results of the field mixture experiments for the background field size of 40’ and 5’. Solid and open symbols represent result for background fields of dia 40’ and 5’, respectively. ( 1) Test of field additivity for the background Jield of Wdia. Each distinct set of data (solid symbols) represents an increment-threshold curve on a different wavelength background: the S.T.

7 10

7

(

1

5

6

Log field Fig.

I

I

7

6

intensity

2. Field-mixture

4

I 9

5

6

I

7 Log

I10

6

quanta (rllS650nm)deg-‘sec

experiment

for

S.T.

9

field intensify

Other

lo 11 (p530nm)

’ dclails

as in Fig.

I

199x

Research Note

periment. The leftmost point was obtained on 650~nm field alone at the intensity specified by an arrow on the 650~nm field axis. The other points were measured with the same 650-nm geld admixed with various amounts of the 530-nm field, specified by the 530-nm field axis. The broken curve is the prediction of field-additivity, based on the Principle of Univariance and the field-quantum-catch hypothesis. formally described by Pugh (1976), Sigel and Pugh (1980). Wandell and Pugh (1980a). The held additivity prediction is given by the equation (Wandell and Pugh, 1980a)

S .T

----0

where Q is log threshold, R,, and n,, are the field sensitivities at the two wavelengths cc, and p?, and I, and I2 are the intensities of the two fields. The field-mixture experiment was executed in 0 10 20 40 30 the Weber’s law region. Therefore, we estimated Diameter ol bac&mund nun ot arc the values of n, and nrt from the increment Fig. 3. lncrrmeat thrcshokJaa a fumion of the dinweter of threshold data for the single monochromatic backgroundfldd. T?tesolid circlesnprcrsn: the increment fields, and calculated the predicted log threshthresholdsupon the monochromaticfield of 6SOnm. The olds for the mixture-field by equation (1). The opencircks repwent the incrementthroahoMupon the field result of the 40’-background field shows the mixture of 650 and 53Onm. Vertical bars denote i: I SE. failure of additivity, for adding flux of the 530-nm field to the 650-nm field lowers the threshold for the 630~nm test. The threshold is the prediction of field-additivity. The field drops by about 0.15 log units for Y.E. (0.2 log mixture data obey this prediction. units for S.T.) from the level upon the 650~nm (3) Field-u&iirivity as a /uncrion of rhe field field alone. This additivity failure of cancel- diameter. Figure 3 shows the additivity property of the 530-650 run field mixtureas a function of lation type is consistent with the results reported by Stemheim et al. (1979) for detection of the background field diametar. The solid symlong-wavelength test lights flickering at low bols represent the increment-thresholds upon a frequencies, and by Wandell and Pugh (1980b) 650-nm field of the same intensity as the GO-nm field in the present field-mixture experiment. for detection of long-duration, long-wavelength The open circles represent the incrementincrement flashes. (2) Tesr of field -addilit:i/y for the background thresholds upon the 530-650nm field mixture, field of dia 5’. Open symbols in Figs 1 and 2 consisting of the same 650-nm field admixed show the increment-threshold data upon the with a 530-nm field whose intensity is specified monochromatic fields for the background field by the arrow on the 530-nm fiakl axis in Figs 1 of dia 5’: the left curve shows data for the and 2. The threshold curves upon the mono650-nm field, and the right curve shows data for chromatic field and the mixture field follow a the 530~nm field. Small background fields are familiar course; the increment threshold demore effective in elevating threshold than the creases as the background size is increased (sensitization) until the function asymptotes. large background fields. This desensitization effect of small fields has been shown by McKee This size effect is known as the Westheimer and Westheimer (I 970) and Buss ef al. ( 1982) effect, An important feature of the present result of the additive property of the Stromeyer (1983). Saturation is not observed in is the dependfield-mixture on the background field size. For the present experiment for the thresholds follow a given size of the background field, the Weber’s law. The field-mixture experiment was field-mixture data point above the curve for the performed using the same field intensity that 650-nm monochromatic field implies the threshwas employed for the 40’ field. The results are old elevation caused by admixing the 530-nm shown by open squares. The intermittent curve

Research Note

field to the 650-nm field, and the data points below the curve indicate the threshold reduction. At the field diameter of 5’, the two components are approximately additive as shown in Figs 1 and 2. Beyond 5, the two components are nonadditive, and field cancellation occurs with large fields of dia 20-40’. DISCUSSION

There is ample evidence for the failure of meld-additivity with Iong-wavelength tests of low temporal frequency or a long-duration. The novel result of the present experiment is that the size of the background field is a significant parameter in determining the field additivity. With large background fields, field cancellation occurs, whereas with small backgrounds, there is ~~ld-additivity. This suggests that adaptation signals, generated by large background fields of different chromaticities, may oppose each other‘s threshold-elevating effects, whereas the adaptation signafs generated by the small background fields show no evidence for such a cone-antagonistic effect. McKee and Westheimer (1970) concluded that there was the cone-specific center-surround antagonism in the long-wavelength detection pathway. Subsequent investigations, however, did not support the conclusion and showed that there were interactions between different types of photoreceptors. Bender (1973) measured the detectability of a red or green probe as a function of diameter of subliminal red or green annuli, and concluded that the sum of long- and middle-wavelength cones affected the excitatory center response. Kelly (I 973) measured contrast thresholds for sinewave gratings under conditions of intense chromatic adaptation, and suggested the spatial inhibition both between and within the red and green mechanisms. Stromeyer (1983) presented further evidence for interaction of signals from different classes of cones based on the analysis of spatial sensitization and desensitization with small adapting lields. Our results showed a clear cone-antagonism for center and surround when we optimized stimulus conditions,

such as tcmporul

paramc-

ter and field intensity. McKee and Westheimer ( 1970) used an exposure time of 10 msec, and Stromcyer (1983) employed a 50-msec duration. Such short-duration flashes are not optimal for

revealing cone-antagonistic and Pugh, 1980a, b).

I999

pathways (Wandell

The present results show that field cancellation has a close relation to the desensitizationsensitization effect of the background fields, In the desensitizing zone (5-10’). field-additivity holds at the smallest field size of 5’. beyond which subadditivity begins to occur. As the background area exceeds approximately IO’, the increment threshold decreases. Field cancellation occurs in this sensitizing zone. The spatial desensitjzation and sensitization function is thought to reflect the center-surround relation of neural receptor field: the decrease in adaptation level with increasing background area is caused by surround inhibition which acts to oppose the center mechanism (Westheimer, 1967; Enoch et al., 1976; Johnson and Enoch, 1976). Therefore, the present finding that the cancellation effect and sensitization effect occur concurrently suggests that a lateral inhibitory interaction may mediate the cone-antagonistic adaptation effect. In the present study, field cancellation is obtained for a very tiny test of 3’, whereas the existing evidence for field cancellation has been obtained for spatially much larger tests (Wandell and Pugh, 1980b; Reeves, 198 1; Stromeyer et al., 1985). It should be noted here that the field-sensitivity measurement taps all the mechanisms that influence test sensitivity, whether they actually comprise the detection pathways or only interact with the detection pathways to desensitize them. Thus, field canccllatjon means the contribution of cone-antagonistic mechanism, but cannot decide whether the coneantagonistic mechanism may comprise one of the mechanisms detecting the test stimulus, or it may reside in channels that interact with, and desensitize, the detection pathways. Recently, Finkelstein and Hood (1982) measured test and field sensitivities with a small, brief test target. and showed that red/green opponent cells could substantially influence the detections of tests of 10’. They proposed a hypothesis of variable tuning of the opponent-color cells, which states that the change in spectral sensitivity of the opponent-color ccl1 is a consequcncc of spatial summation and the center/surround receptive field configuration: large and long-duration stimuli arc mom likely than small and shortduration to activate the surround mechanism

2ooo

Research

(Finkelstein and Hood, 1982; Hood and Finkelstein, 1983). Within this framework, our result indicates that lateral inhibition may come into play when a stimulus is larger than 5--10’. being consistent with the conclusion of Finkelstein and Hood (1982). Arknon~ledgemenrs-This Yamamura

study

Foundation

was granted

was supported

and Tamura

by Nihon

Houso

partly

Foundation.

by

Y. Ejima

Bunka Kikin.

considered Land.

Increment

as signal#oise

visual system. Boynton

R. M..

thresholds at low intensities discriminations.

J.

Physiol..

Spatial

interactions

colour

between the red-

mechanisms

of the

human

lkeda

M.

and Stiles W.

S. (1964)

Inter-

mechanisms

as inferred

from

chromatic

positive and negative increment thresholds. R. M. and Baron W. S. (1982)

Vi.sion Re.c 4.

retmogram. Lateral

Field sensitivity of

mechanism derived from primate Vision

Buss C. M., Hayhoe

local electro-

Res. 22, 869-878. in the control

Finkelstein

Sternheim

C. E.. Stromeyer Visibility

mixed adapting

Changes

of red-,

green-

obtained

on small

and

Newton

blue-sensitive

mechanisms

Vision

Res. 21,

and appearance

E. (1981)

Color coding in primate

Lecture.

M. A. (1983)

A case for the

J. D. and Sharpe

In Co/our L. T.).

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M. C. K

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(1983)

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with small adapting

from

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of sigRc.v

23,

621 -639. C. F. Ill.,

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Wandell

in the red-green

B. A.

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fre-

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chromatic

path-

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Sanchez

J.

Detection

incremental Vision and

of

flashes by a

Res. 20, 625-636. Quinn

B.

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in the long-wavelength

path-

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Note

Sequential

function.

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Br. 1. Math.

SW

18, l-10. G. and Stiles W. S. (1982)

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Co/or Sc,rent?. Wiley.