pupil responses to foveal exchange of monochromatic lights

Pupil responses to foveal exchange of monochromatic lightsRockefeller S. L. Young* and Mathew Alpern

Vision Research Laboratory, The University of Michigan, Ann Arbor, Michigan 48109(Received 21 June 1979)

Temporal exchanges of equiluminant monochromatic lights of different spectral distributions pro-duced a momentary constriction of the pupil in man. This is not a stimulus artifact because ex-changes of two lights with identical distributions in the same apparatus produced no response. Re-sponses evoked by rod signals were successfully obviated by presenting the foveal stimulus inside alarge rod saturating annulus. The amplitude of the response varied systematically with stimuluswavelength. The exchange of a standard light to either shorter or longer wavelength lights produceda momentary constriction of the pupil; the greater the wavelength difference (between them)- thelarger the constriction. This ability to respond to exchanges of one spectral distribution for another isnot a consequence of chromatic aberration or chromatic differences in magnification. Chromaticexchanges between lights of equal chromatic aberration do not produce identical pupillary responsein deuteranopes: The exchange 560 nm -650 nm produced no pupil response, while the 560 nm-498nm exchange produced a sizable response. Exchange of equally luminant heterochromatic lightsevoked a response with 50 ms longer latency than the same amplitude constriction evoked by a stepincrease in luminance of a homochromatic light. The homochromatic contrast needed to evoke thesame constriction as a given equal luminance heterochromatic exchange closely follows the homoch-romatic contrast which matched the residual flicker in flicker photometry of that same wavelengthpair.

INTRODUCTION driven from various parts of the nervous system, including the

The pupil, the aperture stop of the eye, narrows or widens retina. The retinal signals are, in turn, evoked by photonsTh uI hapruesoofteeenarworwds absorbed in rods, cones, or both.1-5according to tension generated by the smooth muscles of the a iiris. Innervated by autonomic nerves, these muscles are When rod signals alone are evoked by spatially superim-

697 J. Opt. Soc. Am., Vol. 70, No. 6, June 1980 0030-3941/80/060697-10$00.50 C 1980 Optical Society of America 697

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FIG. 1. Diagram of the stimulusand recording apparatus. Insertdepicts the stimulus display: a 10circular test field and a 10° an-nular surround.

posed transients of light, it has no meaning to ask what aspectof the change is important. There is only one kind of rod and(like all other photoreceptors of a given kind) it respondsunivariantly. The transient change from one wavelength oflight to a second will, therefore, be silent, provided the lightsare equated for absorption in the rod visual pigment (rho-dopsin).2 Cones are another matter. The normal humanretina contains three kinds. While each responds univariantlyaccording to the absorption spectrum of its own visual pig-ment, their respective signals eventually interact to synthesizeinformation about the change in both the luminance and thechromaticity of the stimulus.

The possibility of evaluating objectively-as well as non-invasively-the nature of the latter is suggested by the ob-servations of Shakhnovich6 and of Clynes and Kohn.7'8 Theyfound that the pupil momentarily narrowed when the stimulusfield was changed from a light of one color to that of another.Because this response occurred even when the two lights hadbeen equated for luminance, there is the possibility that thepupillary constriction was produced by some change instimulus spectral distribution.

Unfortunately, the absence of significant controls for severalpossible artifacts at the transition of the exchange obviatesstrong inferences from these observations. In this paper thematter is studied again, with special attention devoted toexcluding trivial alternative explanations.

1. METHOD

The observer sat in a darkened room with his eyes in theposition shown in Fig. 1. Changes in the left pupil were re-corded by an infrared television pupillometer9 ; very smallevoked responses were averaged by a Computer of AverageTransients. The right eye viewed the stimulus (Fig. 1, inset)in Maxwellian view. The stimulus field consisted of a 100annular surround and a 1° central disc. The annulus was awhite (approximately 3000'K color temperature) 3.38 log scot.td field, which served to saturated the parafoveal rods andminimize possible effects of scattered light from the foveallyfixated central disc. The central disc was monochromatic

(having passed through Baird-Atomic interference filters withhalf-bandwidths of about 10 nm) of about the same luminanceas the annulus.

The observer adapted to the central disc at some standardwavelength, e.g., 490 nm for about 8 s. The standard was thenexchanged for a test wavelength, e.g., 650 nm, for a period of2 s, then returned to 490 nm. This procedure was repeated10 times; each time, the observer's pupillary response wasrecorded and added to the averaged record. (These cyclingparameters were empirically selected to optimize the re-sponses obtained. More extensive experiments by others"have since confirmed this choice.)

Three channels of illumination were lit from the light sourceS (250 W tungsten-halogen lamp). One channel provided thebackground field (the umpolarized channel). The other twochannels were linearly polarized and illuminated the centraldisc. The channel polarized by a vertical polarizer p' pro-vided the standard wavelength. The other, polarized by ahorizontal polarizer pa supplied the test wavelength. Al isthe field stop for the 1° central disc, and A2 the field stop forthe 100 annular surround field. BS, is a beamsplitter cubethat combines the two in a common beam that traverses L,,the Maxwellian viewing lens, and AL an achromatizing lens.L2_1 0 are achromatic lenses; A3_5 are aperture stops; M1_7 firstsurface mirrors; and, BS 2 a pellicle beamsplitter.

The usual screens were required to obviate stray light al-though they are not shown in Fig. 1. These were positionedinitially by the subject to meet the requirement that thetransition from standard to test was invisible when the com-mon beam was covered. As a final check against the possi-bility that stray light leaking to the supposedly unstimulatedeye on exchange caused the pupil response, the test beampresentation to the right eye was totally occluded and thepupil response of the left eye to standard-test exchange wasstudied. No response could then be recorded.

The exchange between the standard and test wavelengthin the central disc was accomplished by rotating a linear po-larizer p through a 900 angular step in the common path of the

Rockefeller S. L. Young and Mathew Alpern 698698 J. Opt. Soc. Am., Vol. 70, No. 6, June 1980

p' and p" channels. When the common polarizer was in theO position, only horizontally polarized light (test wavelength)emerged. Conversely, in the 90° position, only the verticallypolarized light (standard wavelength) was transmitted. [Theextinction ratio of the polarizers in series was less than 6.00X 10-3 between 490 and 650 nm. The transition time for the900 step was 40 ms. No overshoot in angular position of thestepper (American Electronic, Model 1 1S20J 15) could bedetected.]

Theoretically, if the luminances of the standard and testwere equated, the luminance of the central field should notchange during the transition from the standard to the testwavelength. In practice, however, additional precautionswere needed to ensure that isomeric exchanges would beperceptually silent. First, careful alignment of the twochromatic channels was necessary to eliminate perceivedmovements in the central field during the wavelength ex-change. Second, an achromatizing lens was placed in frontof the observer's right eye to minimize the effects of axialchromatic aberrations of the eye.12 Third, the points ofpupillary entry of the standard and test wavelength beamswere carefully superimposed.

In addition, a quarterwave retardation plate whose axis wasset at 450 to that of the linear polarizer was attached to therotating polarizer between the latter and the eye. Using thequarterwave plate in this manner, we observed that the lightemerged circularly polarized. The conversion to circularlypolarized light helps to obviate two other sources of artifact:(i) any residual sensitivity of the eye to changes in orientationof linearly polarized light13"14; and, (ii) partial polarizationimposed by reflection and refraction in the optical compo-nents between the rotating linear polarizer p and the eye.

To measure the action spectrum of the photopupil response,a 2-s flash of monochromatic light was exposed at various in-tensities to the eye adapted to the surround annulus. Suc-cessive flashes followed one after the other with 8 s intervalsinterspersed between flashes during which the centrally fixed10 test area was dark. Tests were carried out at 16 differenttest wavelengths spanning the spectral range 490-650 nm inapproximately 10-nm steps. Responses matched in ampli-tude irrespective of the test wavelength were essentially iso-bolic (i.e., superimposable). At each wavelength, curves wereplotted illustrating the relation between test intensity andmagnitude of some feature of the response (latency, maximumamplitude, etc.). In the main, curves of this kind obtainedfor the same feature at different wavelengths superimposedwhen shifted along the intensity axis (an exception was themaximum amplitude at 650 nm, which was slightly moresensitive at high flash intensities than expected from this rule).Action spectra were obtained by determining the intensity ofa flash required at every wavelength to produce a constantresponse criterion.

By running the stepping motor continuously, the test areawas made to alternate in the range of subjective flicker ap-propriate for flicker photometry (12.5-20 Hz). At every testwavelength in the 490-650 range the intensity of the test wasadjusted to minimize the flicker between it and a fixed stan-dard. In most cases this procedure was followed at the be-ginning of each experimental session for all wavelengths to beexamined for the pupil during that session in order to be cer-

EXCHANGE WAVELENGTHS(nm)

490-650

650-490

490-490

0.25mm

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0.5sFIG. 2. Representative records of pupil responses to chromatic ex-changes. Observer, R. Y. The exchanged wavelength pairs are given justto the left of the start of each trace. Each curve is the coherent averageof 10 trials.

tain that the two exchanges of light had, in fact, the same lu-minance. For subjects with laboratory time constraints, thepsychophysical measurements were completed in a separatesession. In either case the results of these matches after ap-propriate calibration could be used to calculate the observer'sheterochromatic spectral luminosity curve as determined byflicker photometry.

The resulting curves for the subjects of this experimentagree reasonably well with the C.I.E. photopic luminositycurve. The principal subject of these experiments is slightlyless sensitive in the long-wave spectral extreme than thestandard observer, but giwen his normal color vision and thewide individual differences of the observers from whom theC.I.E. curve was derived, no significance is attached to thisdiscrepancy.

II. RESULTS

Figure 2 shows representative pupillary responses to either490 - 650 or 650 - 490 nm equiluminant exchanges. Uponexchanging the two chromatic lights, after about a 0.5-s la-tency, the pupil constricted momentarily with an amplitudeless than 0.5 mm. The pupil then widened back toward itsoriginal diameter. Each tracing shown is the average of 10consecutive trials and was obtained on separate experimentalsessions. The pupillary responses in this and other figures(unless otherwise stated) were of R. Y., a 29-year-old, color-normal male. Similar responses were also recorded in G. Y.,a 28-year-old female and in K. K., a 36-year-old male, bothwith normal color vision.

To test whether the pupillary constriction was caused bya stimulus artifact, e.g., a luminance transient or an auditorycue time-locked to the stimulus, the pupillary responses werealso recorded to exchanges of lights of identical wavelength


composition. (Such "isomeric" conditions were achieved byplacing an interference filter between the rotating polarizerp and the field stop Al.) If the pupillary constriction resultedfrom some artifact, the constriction should also occur to ex-changes of identical-as well as to different-lights. How-ever, Fig. 2 (bottom) shows that the exchange of identicallights did not cause a consistent pupillary response.

An important feature of these responses to equiluminantheterochromatic exchanges is that they are unidirectional, i.e.,either 490 - 650 or 650 - 490 in Fig. 2 results in constriction.This result is reminiscent of Clynes's observation' 5" 6 that thepupil constricts both to a pulse of light and a pulse of dark;indeed, it was the theoretical treatment of the latter phe-nomenon that led to the discovery with which this paper deals.Our limited experiments with homochromatic exchanges ofdifferent intensities also confirms the nonlinearity observedby Clynes in that the step-up of a given increment generallyproduces a larger constriction than the dilation produced bya step-down of the same amount. The extent to which thisphenomenon can be related to asymmetries that depend uponthe absolute size of the pupil at the moment of exchange'requires more attention than we have so far been able to de-vote to. In the analysis of the present results, the small di-lation that occurred at the substitution of a monochromaticlight of one wavelength for a slightly weaker light of the samewavelength was usually ignored and only constrictions eval-uated. This facilitated decisions about responses near theisometric point of homochromatic exchanges, but numericallybiased the average value of several repetitions of the mea-surement of such responses in favor of constriction.

To what extent are the responses to equiluminant hetero-chromatic exchanges shown in Fig. 2 attributable to a recti-fied luminance signal evoked by inappropriate brightnessmatch, as could occur if two lights equated by flicker pho-tometry were not equally effective in driving the pupil? Thispossibility can be excluded for two reasons. In the first place,unequally matched homochromatic lights do not drive thepupil with a completely rectified signal since a step decrementcauses a dilation, and an increment a constriction. In thesecond place, the action spectrum of the pupil response toflashes agreed well (within 0.1 to 0.2 loglo unit margin of ex-perimental error) with the subject's luminosity curve mea-sured by flicker photometry independent of the criterion(maximum amplitude value, latency, etc.) of the former em-ployed. Discrepancies within this margin of error werechecked by observing responses to the exchange of lightsequated for photopupillomotor spectral sensitivity; these werealways just as effective in producing the results as were ex-changes in which the lights were matched by flicker pho-tometry.

Consider next the possibility that the exchange fromequiluminant short- to long-wave light excites cones while theopposite exchange excites rods. This is unlikely because abright (3.38 log scot. td) annular surround was used to elimi-nate possible stray light effects that could cause light focusedon the rod-free fovea to excite parafoveal rods. The effec-tiveness of this annulus was demonstrated in the followingways.

First, as already noted, the action spectrum of the pupillaryresponse agreed with the flicker photometry curve obtained

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FIG. 3. Top: Amplitude (+ 1 SEM) of the pupillary exchange response(650 - 490) as a function of time in the dark after a 30% bleach. Themean amplitude of constriction during the cone plateau period was 0.37+ 0.02 mm and 0.35 + 0.02 mm during the rod plateau (n = 15). Middle:Psychophysical dark-adaptation curve determined in the parafovea (50eccentricity), without annulus. Bottom: Changes in steady pupil diameteras a function of time in the dark after a 30% bleach.

in the observer's fovea. Both curves were photopic. Second,the pupil responses to chromatic exchanges during dark ad-aptation were evaluated. Responses to equiluminant 650- 490 exchanges were obtained during two periods in the darkfollowing a 30% bleach (Fig. 3 top). If evoked by rod signals,the response amplitude during the 1200-1800 s (20-30 min)period should be greater than during the 180-480 s (3-8 min)period, because rod sensitivity is greater during the formerthan during the latter period. However, there was little or nodifference in the pupil responses during the two periods (Fig.3, top). The pupil amplitude was 0.37 I: 0.02 mm over the 3-8min period, and 0.35 i 0.02 mm (x At 1 SEM.; n = 15) over the20-30 min period. Figure 3 (middle graph) shows a psycho-physically determined dark-adaptation curve at 50 eccen-tricity (without the annular surround). This graph verifiesthat, in this observer, the cones recovered full sensitivity after6 min whereas the rods recovered after about 20 min. Figure3 (bottom) shows that, after about 3 min, the absolute size ofthe pupil was constant as a function of time in the dark fol-lowing the 30% bleaching, hence potential artifacts attribut-able to differences in absolute pupil diameter' 7 are not re-sponsible for the result.

Third, responses to these exchanges show the directionalsensitivity of cones, not rods (Fig. 4). The response amplitudeto the 650 - 511 exchange was measured as a function of theintensity of both members of the exchange pair, alwaysequiluminant, entering the eye through the center of the pupil

Rockefeller S. L. Young and Mathew Alpern 700

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700 J. Opt. Soc. Am., Vol. 70, No. 6, June 1980

(Fig. 4, upper right). The responses were then recorded whenthis light entered the eye through different parts of the pupil(Fig. 4, upper left). This experiment was repeated five times,and the mean amplitudes (with the aid of the template curvein in the upper right-hand graph) were used to determine thedirectional sensitivity of the pupil response evoked by theexchange (Fig. 4, lower half). The ordinate is relative lumi-nous efficiency, log ?7/?lmax, where w7 is the equivalent 650

511 luminance estimated from the template curve.

These results are in good agreement with the directionalsensitivity properties of cones: The parabolic smooth curvedrawn through the points in the bottom graph of Fig. 4 has thesame form and magnitude that Stiles' 8 found to describe thepsychophysical estimates of the directional sensitivity of hisown foveal cones to monochromatic lights. Rods, on the otherhand, are nearly insensitive to which part of the pupil lightenters the eye.

Figure 5 illustrates the pupillary responses to chromaticexchanges of equal and unequal luminances. The pupillaryresponses at the top were obtained when the test intensity wassystematically varied while the intensity of the standard re-mained fixed. (The standard wavelength was 490 nm; thetest, 650 nm). The first record is the exchange response from490 nm to a very dim 650; the bottom record is to a bright 650.The arrow indicates the exchange of equiluminant lights. The

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FIG. 4. Directional sensitivity of the pupil constriction evoked by equilu-minant heterochromatic exchanges. Top right: Curve shows the amplitudeof the X1 - X2 response, when the intensity of both XI and X2 werechanged together (central pupil entry). Top left: Responses evoked whenthe same exchange entered the pupil at the indicated position. The graphin the lower half shows the luminous efficiency of the pupil response de-termined from the relative luminance needed to equate the response withone that was evoked by light entering the center of the pupil. The smoothcurve has the equation log 17/frmax = p(r - rmax)

2 of a parabola which de-scribes the directional sensitivity of foveal cones measured psychophysi-cally.18 In the figure, the constant p = -0.07 and rme, = 0.13 mm superiorpupil; X1 = 650 nm, X2 = 511 nm.

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FIG. 5. Below: Representative response series illustrating how the pupilresponse varies as a 490-nm light is exchanged for different test wave-lengths and luminances. Arrows indicate the flicker photometry equationvalue. Above: Representative responses making up the right-hand set(XI = 490 nm, X2 = 650 nm). Note that no obvious null, such as is foundin the homochromatic exchange, can be found as the intensity of the 650-nmlight is reduced.

bottom graph (Fig. 5) plots the amplitude of the pupillaryconstriction as a function of test intensity, with test wave-length varied parametrically, the standard wavelength always490 nm. The arrows in each case point to the relative inten-sity (determined by flicker photometry) that equated the testwith the standard luminance.

Three interesting features can be observed in Fig. 5. First,the occurrence of the pupillary constriction does not criticallydepend on an exact luminance match. For example, thepupillary constriction to the 490 - 650 exchange occurredeven when the test is more than 0.5 loglo units dimmer thanthe standard. Second, the amplitude of constriction increasedmonotonically with increase in test intensity. Third, theamplitude of constriction for equiluminant exchanges (asindicated by the arrows in the bottom graph of Fig. 5) ap-peared to vary with test wavelength. The amplitude was zerowhen the test and standard wavelengths were identical, andwas largest when the difference between test and standardwavelengths was maximal.

Figure 6 quantifies more extensively the relationship be-tween amplitude of pupillary constriction and the wavelengthsof equiluminant exchanges. In each plot, the open circlesrepresent the response amplitudes (mean of 5 replications)


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to XI - X2 exchanges; the solid circles, X2 -A X exchanges.Several points are of interest. First, the exchange betweenlights of identical wavelengths yielded little, if any, pupillaryresponse. The response to this condition corresponds to theminimal point in the curve of each graph. Second, when theexchange was between nonidentical wavelengths, the pupilconstricted. The constriction seems to be a function of thedifference in the standard and test wavelengths. The greaterthe difference, the larger is the amplitude. Third, the ex-change of a standard wavelength in the middle of the spec-trum, e.g., 571 nm, to either shorter or longer wavelengthsproduced pupillary constriction. These three points are ap-plicable to each of the graphs in Fig. 6.

What is the action spectrum of lights required to null theexchange for any given XA? It is not easy to answer thisquestion experimentally because as the intensity of X2 wasvaried spanning the range between lights that produce cleardilation and crisp constriction, there was no value at whichthe pupil remained immobile to the substitution. Instead,there was a range of test intensities in which both a dilationand a constriction occurred in response to any given Xi - X2exchange (Fig. 5, top).

To obviate this difficulty, action spectra were determinedfor a small but unequivocal constriction, at a variety of stan-dard wavelengths. The results are illustrated in Fig. 7. Thesegraphs show for six different XA wavelengths the relative

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photon sensitivity required to produce a fixed 0.1 mm con-striction at the X2 substitution. The curves are quite irregularin shape and are not easily describable by some simple alge-braic combination of the most probable absorption spectraof this subject's foveal cone pigments, even granting adapta-tion effects following some variant of the von Kries coefficientslaw.' 9

The results described above were all obtained on color-normal observers. The pupillary responses in three deuter-anopes were also investigated. The results for one deutera-nope are shown in Fig. 8; similar results were found for a sec-ond deuteranope. The third did not have a foveal, pupillarylight reflex, and results could not be obtained on him. Re-sponses in three conditions were studied: (i) to red - green(560 - 650 or 650 - 560; (ii) to blue - green (560 - 498 or498 - 560); and, (iii) to neutral point (white - 498) ex-changes. All stimulus exchanges were equated for luminanceby the observer prior to the recordings. As shown in Fig. 8,the pupil of the deuteranope did not react to the red - greenexchanges, but did respond to the blue - green exchanges.In addition, his pupil responded to white - 511 or white

- 490, but not to white - 498 (i.e., his neutral point ex-change).

The achromatizing lens AL is, no doubt, an effective, thoughperhaps not perfect, control for axial chromatic aberration.But it does not correct for chromatic differences in magnifi-cation. Hence the possibility exists that the pupil responsenormally found is evoked by the change in the focus or the sizeof the XA and X2 images. The results in Fig. 8 exclude thesepossibilities.

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TABLE 1. Comparison of the latencies of equal-amplitude responses evoked by equiluminant heterochromaticluminant homochromatic exchanges.

exchanges to those evoked by unequally

Hetero Homo Test of Hetero Homo Test ofchromatic chromatic differencea chromatic chromatica differencea490- 650 650- 650 t p 650 - 490 490- 490 t p

Amplitude Mean 0.2574 0.2520 0.25 N.S.b 0.2394 0.2436 0.16 N.S.(millimeters)

Std. Dev. 0.0469 0.0371 0.0445 0.0446Latency Mean 0.5202 0.4825 2.56 <0.05 0.5423 0.4760 4.5 <0.001(seconds)

Std. Dev. 0.0283 0.0281 0.0253 0.0265N 7 10 6 9

a Students' t test (two tailed) of difference between the hetero- and homochromatic means.b N.S. = Not significant.

For the average eye,12 the differences in chromatic aber-ration between 560 and 650 nm are about the same as thosedifferences between 498 and 560 nm, and as shown in Fig. 6,the exchange between the former pair evokes only a slightlylarger pupil constriction than the exchange between the latterpair for the normal eye. If this response were evoked by aluminance signal excited by the differences in focus or imagesize at the exchange X -> X2, the 560 - 650 exchange shouldbe somewhat more effective for the deuteranope than the 498- 560 nm exchange, just as it was in the normal eye (Fig. 6).On the contrary, the results (Fig. 8) demonstrate that the 560- 650 exchange evoked no response, while the 498 - 560evoked a response as vigorous in the deuteranope as it did inthe normal.

Rushton2 0 and Alpern and Wake2l provide strong evidencethat deuteranopes are missing a middle-wave-sensitive conevisual pigment. It is generally agreed that short-wave-sen-sitive cones make little or no contribution to the matches madein flicker photometry. The fact that an exchange betweenequiluminant (X1 = 498 nm, X2 = 560 nm) lights, or for thatmatter, between a white light and a monochromatic light notmetameric to it, evokes responses in deuteranopes, is goodevidence that something other than luminance signals mustbe involved. These results prove that absorption of photonsin both long- and short-wave-sensitive cones can evoke theresponses under study. However, if the 498 - 560 responseis mediated by the short- and long-wave cones and if the 560- 650 response (absent in the deuteranope) is mediated bythe long- and middle-wave-sensitive cones, it follows that thenormal trichromat's responses, whose amplitudes are shownin Fig. 6, must be mediated by the photons absorbed in allthree foveal cone mechanisms.

How do the pupil responses to equiluminant heterochro-matic exchanges compare to those evoked by homochromaticluminance exchanges? Since the form of either responsedepends upon the strength of the exchange, any two such re-sponses to be compared must have the same maximum am-plitude. Evaluation of the results already described suggeststhat any such differences would be very small and best re-vealed when the X1, X2 components of the heterochromaticexchange were the spectral extremes.

A series of responses were recorded to equiluminant 650490 (and vice versa) exchanges and to 490 nm (or 650 nm)

homochromatic exchanges in which the second member of the

exchange was made 0.2 loglo units brighter than the first (i.e.,to yield responses of amplitudes equal to those of responsesevoked by heterochromatic exchange). Even with this con-straint many of the responses to the homochromatic lumi-nance steps fell outside the range of amplitudes obtained withthe equiluminant heterochromatic exchange and had to berejected. The results were obtained on a single observercollected over two days with several experimental sessions perday.

The results were analyzed in terms of the response latencydefined as the time between the stimulus exchange and theresponse onset which was measured by the intersection of thebase line and the line tangent to the constriction phase of theresponse (see Table I). From these results, it is evident thatthe responses evoked by the homochromatic luminance stepbegan, on the average, about 50 ms before a response of thesame amplitude produced by the exchange of equiluminantheterochromatic lights. This means that the two responsesdid not have identical time courses.

To get some idea as to how their waveforms differed, fourrepresentative responses from each of the four conditions weredigitized and averaged at 50-ms time intervals (Fig. 9). In (a),the average response to the 650 - 490 exchange (open circles)is compared to the average response evoked by the homo-chromatic (490) exchange (filled circles); in (b), the oppositesets are compared. In each case the response evoked by theheterochromatic exchange began later and developed at a

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FIG. 8. Pupil responses to exchange of equiluminant heterochromaticlights for deuteranope M.T. Above: Responses to monochromatic lights;below: exchange between a white light and monochromatic lights at, aswell as on either side of, this subject's neutral point.


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FIG. 9. Comparison of equal amplitude pupil constrictions evoked byequiluminant heterochromatic exchange (open circles) and by a homo-chromatic luminance step (solid circles). In A, XA was 650 nm or 490 nmand X2 was always 490 nm; in B, X, was 490 nm or 650 nm, and X2 wasalways 650 nm.

slightly faster rate than the equal-amplitude responses evokedby the homochromatic luminance step. [In retrospect thesesubtle differences in time characteristics can be related to thewaveforms shown in Fig. 5 (top). When \ 2 (650 nm) was inthe range 1.96-1.51 the pupil appears first to dilate to the lu-minance of \ 2 and then to constrict to its chromaticity.]

That the exchange of two equiluminant lights makes thepupil constrict reminds one of electroretinogram (ERG) andvisual evoked response (VER) responses evoked by counter-phase shifts of equiluminant heterochromatic bar patternsdescribed by Riggs et al.2 2'23 Even more familiar is the clas-sical psychophysical observation that equating the luminanceof two lights of different colors does not eliminate all flickerwhen they are alternated in flicker photometry. Are thesignals responsible for all three of these effects the same?

Available evidence does not provide a definitive answer tothis question. However, the recent experiment of Boyntonand Kaiser24 suggests a way this could be done. They mea-sured the magnitude of residual flicker in heterochromaticflicker photometry by adjusting the depth of modulation (andhence, the contrast) of homochromatic (650 nm) flicker untilthe two residual flicker effects matched. Their results forthree observers relating the equivalent homochromatic con-trast (Bmax - Bmin)/(Bmax + Bmin) and X2, in the 580 - 2flicker, are plotted in Fig. 10 (bottom). They can be compareddirectly with analogous pupil responses evoked by equilumi-nant heterochromatic exchange (Fig. 6, upper right). All thatis necessary is a template curve of the homochromatic (650nm) exchange in which the amplitude of the responses evokedby various Bmin - Bmax exchanges are given. The top insertof Fig. 10 shows precisely this template curve, the abscissa ofwhich is log Bmax/Bmin. The obtained pupil data plotted asopen circles in the graph of Fig. 10 (bottom) are in goodagreement with the flicker photometry data of two of the threeobservers of Boynton and Kaiser. The approximate agree-ment shown in this comparison suggests the possibility thatthe signals evoking the pupil response to heterochromaticexchange and those leading to the perception of residualflicker in flicker photometry have the same underlyingphysiology.

111. DISCUSSION

Kohn and Clynes8 modeled the photopupillary responsewith two constituents: (i) a unidirectional rate sensitivecomponent which only causes a constriction upon the step-upin photon absorption in any photoreceptor type; and, (ii) abidirectional component causing a constriction to a step-upand a dilation to a step-down in photon absorption. Unfor-tunately, the model does not account for the crisp constrictionKohn and Clynes found to the removal of, say, a red test froma green background. To deal with this difficulty they ad-vanced an ad hoc hypothesis (mutual inhibition between thereceptor types excited by their red and green lights) the the-oretical implications of which are difficult to examine untilits details are made quantitatively more explicit.

A simple alternative is to suppose that the retinal signalsto the pupil are triggered both by stimulus luminance andstimulus chromaticity. The signal for the latter is rectifiedso that whenever a stimulus of one chromaticity is substitutedfor another the pupil constricts, but the signals for the formerproduce either a dilation or a constriction depending uponwhether the luminance has decreased or increased, respec-tively. This idea is consistent with all the available evidence

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FIG. 10. Top inset: Response amplitude to a 650-nm luminance step asa function of the logarithm of the luminance ratio of the second to first light.Below: Comparison of the equivalent homochromatic contrast neededto match the residual flicker in heterochromatic flicker photometry (hexagon,diamond, and square from Boynton and Kaiser24) with that required to matchthe pupil constriction to exchanges with a 580-nm standard (open circles).The results from the top right graph of Fig. 6 were transformed using thetemplate shown in the top inset. The smooth curve below shows the trendsof the pupil responses.


01


and deals with the variety of action spectra obtained for0.1-mm constriction (Fig. 7) in a simple and straightforwardway. But with it the photopupillary unidirectional ratesensitivity to achromatic stimuli must be attributed to thenonlinearities of the luminance signal alone, about which agood deal more needs to be learned before experimental at-tempts to exclude it can be undertaken.

That the optic nerve signals luminance and chromaticityalong separate channels is certainly the prevailing physio-logical view of visual psychophysicists who deal with color.Unfortunately, there is little in the way of hard physiologicalevidence to give it much substance. Luminance and chro-maticity are important psychophysical constructs but theirneural correlates, if any, remain unclear. "Broad-band" ac-tion spectra have been recorded from retinal ganglion cells andlateral geniculate neurons as well as from cells elsewhere inthe visual nervous system, but their significance is not at allwell specified. In this paper the concept of luminance signalis introduced as a hypothetical construct to account for thepupil constriction evoked by a step-up in the intensity of amonochromatic light and for the dilation evoked by a step-down in its intensity. Similarly, the hypothetical constructthe chromaticity signal is proposed to drive the pupil con-striction evoked by the exchange of heterochromatic lights ofthe same luminance. Most psychophysicists and even someelectrophysiologists speak of "color coded" opponent ganglioncells, but again the evidence that such cells carry a color-codedmessage is at best equivocal.

If these color opponent and broad-band cells do, in fact,provide the physiological bases for the constructs introducedhere, it is clear that the small differences in their conductionvelocities25-2 7 will not account for the 50 ms or so latencydifferences shown in Fig. 9, subtle as those differences maybe. This, in turn, raises the real possibility that photopupilresponses evoked by equiluminant heterochromatic exchangesmay be produced by signals that are not a part of the ordinarypupillary light reflex, but on the contrary, must first travel tovisual cortex before descending to the pupillomotor nuclei ofthe midbrain. The matter needs evaluation on corticallyblind persons with normal pupil reflexes.

According to the psychophysicist's conventional view,color-coded retinal signals are of two types: red-green op-ponent and blue-yellow opponent. If together they providethe chromaticity signals for the pupil response, it is easy to seethat these signals are by no means the only way informationabout stimulus color is carried to the visual central nervoussystem: The exchange of a blue light (which is uniquely bluein the sense of Hering opponent theory) for an equiluminantunique yellow light invokes a constriction virtually identicalto that evoked by the yellow for blue exchange. Hence theserectified "opponent" signals do not distinguish the two ex-changes; but the brain clearly detects the difference, seeingthe substituting light as blue in the first instance, and yellowin the second. Evidently, to preserve the conventional viewit is necessary to postulate a rectification which cannot bemade general either for all "chromaticity" signals or for allsignals for photopupil constriction.

After the original version of this paper was submitted to thisjournal, it published a description of the experiments of Sainiand Cohen,"1 the results of which were until then unknown

to us. Those results are fully compatible with our ownwhereever the two sets overlap, although by working with alarger field Saini and Cohen obtained much larger pupil re-sponses, at the cost of exciting an additional photoreceptormechanism (i.e., rods). This is a complexity we have takensome pains to obviate. On the theoretical side they haveelected to follow and extend the original scheme of Kohn andClynes. 8 Hence their theory differs in detail from thatadopted here in a way that should be sensitive to experimentalchoices between them. Specifically, we find it difficult tosuppose that a step-down in rod photon absorption in isolationwould not lead to a pupil dilation, unless the pupil immedi-ately prior to the step was already at, or very near, its maxi-mum size. Clearly further experiments are required.

ACKNOWLEDGMENTS

This research was supported by NIH Postdoctoral Fel-lowship (to Rockefeller S. L. Young) No. 5 F22 EY00097 andby research grant EY-00197 (to Mathew Alpern). Supple-mentary work done after the fellowship was supported in partby NIH Training Grant EY703802 and by a Manpower Awardfrom the Research to Prevent Blindness, Inc.

We thank G. Wyszecki for the gift of the lens which cor-rected for the chromatic aberration of the eye.

*Now at Illinois Eye and Ear Infirmary, Room 3. 164, 1855 W. Taylor,Chicago, Illinois 60612.

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5M. Alpern, N. Ohba, and L. Birndorf, "Can the response of the iristo light be used to break the code of the second cranial nerve inman?," in Pupillary Dynamics and Behavior, edited by M. P.Janisse (Plenum, New York, 1974), pp. 9-38.

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and communication," Ann. N.Y. Acad. Sci. 92, 946-969 (1961).16 M. Clynes, "The nonlinear biological dynamics of unidirectional

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23 L. A. Riggs and C. E. Sternheim, "Human retinal and occipital po-tentials evoked by changes of the wavelengths of the stimulatinglight," J. Opt. Soc. Am. 59, 635-640 (1969).

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26 B. Dreher, Y. Fukada, and R. W. Rodieck, "Identification, classi-fication and anatomical segregation of cells with X-like and Y-likeproperties in the lateral geniculate nucleus of old-world primates,"J. Physiol. 258, 433-452 (1976).

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706 J. Opt. Soc. Am., Vol. 70, No. 6, June 1980 0030-3941/80/060706-06$00.50 C 1980 Optical Society of America 706

pupil responses to foveal exchange of monochromatic lights

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