Transient and sustained components of the pupillary responses evoked by luminance and color

Vision Res. Vol. 33, No. 4, pp. 431-446,

W2-6989/93 56.00+ 0.00 Copyright 0 1993Pergamon Press Ltd

1993

Printed in Great Britain. All rights reserved

Transient and Sustained Components of the Pupillary Responses Evoked by Luminance and Color ROCKEFELLER

S. L. YOUNG,*

BAE-CHEOL

HAN,? PING-YUAN

WU*$

Received 16 March 1992; in revised form 13 August 1992

That the pupil reacts to changes in luminance and color, as well as to spatial features in the retinal image raises questions about whether phasic and tonic and/or color and luminance visual pathways project to the pretectal pupillomotor neurons. The present study compares pupillary responses evoked by heterochromatic and achromatic luminance increments to investigate whether the pupillary responses evoked by color and by luminance are independent of one another. Principal component analysis is used to examine the constituents of the pupil responses. The results support the belief that the visual input to the pupillomotor system is organized into phasic and tonic (but not necessarily independent color and luminance) pathways. Pupillary

light reflex

Luminance

Color

Phasic and tonic pathways

INTRODUCTION

In primates and humans, a retinal image is densely sampled by parallel visual pathways. How these pathways are involved in the analysis of an image and how they are distributed among different processing streams are topics of current interest. Much research has been devoted to studies of the pathways to the visual cortex, including the phasic broad-band (or M-) and tonic color opponent (or P-) pathways, and to their role in the perception of luminance, color, form, and motion (e.g. Livingstone & Hubel, 1988; Merigan, 1989; Lennie, Trevarthen, Van Essen & Wassle, 1990; Schiller, Logothetis & Charles, 1990; Shapley, 1990; Rodieck, 1991). Relatively less effort has been directed toward studies of the visual pathways projecting to oculomotor nuclei and to their role in such visuomotor reflexes as pupillary light reflex. Neither anatomical nor electrophysiological studies have identified which visual neurons project to the pretectal pupillomotor centers in humans or primates. The identification of these visual neurons is complicated by the fact that the pretectum contains a cluster of nuclei, of which only a few are actually involved in the pupillary response (Trejo 8z Cicerone, 1984), and by the possibility that the pupillomotor nuclei may also receive visual input from the occipital cortex as well as from the retina (Barbur & Forsyth, 1986). Studies

have shown, however, that the phasic broad-band pathway in monkeys does project to oculomotor nuclei, including the superior colliculus and pretectum (Schiller & Malpeli, 1979; Leventhal, Rodieck & Dreher, 1981), although the broad-band pathway may only represent a minor projection (Perry & Cowey, 1984). There is no evidence that the tonic color opponent pathway projects directly to these nuclei. Functionally, the human pupil behaves as if it were predominantly driven by luminance signals. The steadystate pupil diameter varies systematically with stimulus luminance, decreasing (constricting) when luminance is raised and increasing (dilating) when luminance is lowered. To a first approximation, the diameter vs luminance relationship is univariant over a wide range of stimulus wavelengths. The action spectrum of the pupil response is broadly tuned and can be described by a weighted combination of the CIE scotopic and photopic luminosity efficiency functions (e.g. Alpern & Campbell, 1962). But there are additional (albeit, less frequently cited) observations which suggest that the visual input to the pupillomotor nuclei may be more extensive than just luminance signals and may be similar to the input to the visual cortex. First, the pupil also reacts to changes in the chromaticity (e.g. Kohn & Clynes, 1969; Saini & Cohen, 1979; Young & Alpern, 1980) or in the spatial frequency composition (e.g. Ukai, 1985) of the retinal image. Second, night vision sensitivity (e.g. Stewart & Young, 1989) and visual acuity (e.g. Slooter & van Norren, 1980; Barbur & Thomson, 1987) derived from pupillary responses are nearly identical to sensitivity and acuity determined perceptually by the observer. Third, the pupil response behaves as if it were composed of

*Department of Ophthalmology and Visual Sciences, Texas Tech University Health Sciences Center, Lubbock, TX 79430-0001, U.S.A. TDepartment of Industrial Engineering, Texas Tech University, Lubbock, TX 79430-0001, U.S.A. SVisiting ophthalmologist from Shanghai Sixth People’s Hospital. 437

transient and sustained components. When evoked by scotopic luminance steps (e.g. Lowenstein & Loewenfeld, 1969) or by isoluminant color exchanges (e.g. Kohn & Clynes, 1969), the pupil response is purely transient. That is, the pupil constricts momentarily and then returns to its original diameter even though the stimuIus is still present. When evoked by large luminance steps, the response is sustained over the duration of the luminance step. To account for the transiency and sustenance of pupillary responses, the pupillary light reflex has been modeled with two independent processes, a unidirectional, rate-sensitive process and a proportional process (Clynes, 1961; Kohn & Clynes, 1969). The rate-sensitive process filters information about the temporal changes, while the proportional process filters information about the steady-state features in the retinal image. Thus, each time the retinal image is changed, the model predicts that the subsequent pupillary response will be composed of two components, a transient response component whose amplitude is related to the rate of change in color, luminance, spatial frequency etc., and a sustained response component whose amplitude is related to the steady-state quantity of the same image features. The present study builds upon the idea that the pupillary light reflex may be mediated by multiple, independent processes. However, in contrast to Clyne’s model, we consider the possibility that the pupillary processes may be organized along lines more similar to the perceptual visual pathway, for example, organized along phasic and tonic pathways (e.g. Gouras, 1968) and/or color and luminance pathways (e.g. King-Smith & Carden, 1976). Our framework focuses on whether different pupillary processes that are specific to stimulus changes or steady-state stimulus features might also have preferences for other stimuIus aspects such as luminance or color. Our study uses two new approaches. The first approach compares the responses evoked by heterochromatic and achromatic luminance increments. Because the heterochromatic luminance increment produces both a color change and a luminance increment whereas the achromatic luminance increment produces only a luminance increment, the comparison is expected to provide info~ation about how the pupil responses evoked by color combine with those evoked by luminance. The second approach uses principal component analysis to examine whether the nature of the pupil responses evoked by the heterochromatic and achromatic luminance increments are different. GOODS Subjects

The subjects were graduate students and staff members with normal vision correctable to 20/20 or better. Subjects A, B, and D were emmetropic. All three were men, ages 34, 31, and 23 yr, respectively. Subjects C and E were myopic, both requiring about 5-6 spherical D of correction. Both were women, ages 25 and 43 yr, respect-

ively. All subjects had normal color WSIOII ;II!CI mtnc wer‘~~ on medication during the testing period. In!ortnrcl l*oli sent was obtained prior to the start 01‘th(: >tucis.

Subjects dark-adapted for at least 30 min prior to the pupil recording. The subjects were seated with their heads held in position by a chin and forehead rest. In the experiments reported here. subjects viewed the stimulus, a Macintosh II color monitor. monocularly from ;I distance of about 700mm. The pupil diameter of the same eye was recorded using an i.r. video pupil tracking system (ISCAN model 416). The fellow eye was patched. In ancillary experiments. subjects A and R were also tested while viewing the stimulus through a 3 mm apcrture with one eye as the pupillary response> were recorded consensually from the unstimulated fellow oyc. As results from this experiment were qualitatively similar, results for the remaining subjects were only obtained using the monocular testing procedure. The computer-generated stimulus was dispfaycd with a video frame rate of 67 Hz. The stimulus field was spatially homogeneous except for minute tixation points in the center of the field. The field subtended about 18.5 horizontally and 14.5 vertically. Temporal changes in the stimulus were calibrated using a PIN-IOSR photodiode. The stimulus luminance and chromatictiy wcrc calibrated using a Minolta (2150) TV Color Rntrly~cr. The pre-stimulus luminal~ce was slightly different for each subject, ranging from 13.8 to 16.0 cd/n’. The colors used in the experiment were ‘-white” and “purplish”. The C.I.E. chromaticity coordinates of the white field were .Y= 0.273 and J‘ = 0.328. The chromaticity coordinates of the purple field were as follows: subject A (0.392, 0.190), B (0.362, 0.177). C (0.370. 0.1X1). D (0.384, 0.189). and E (0.343. 0.167). The exact luminances and chromaticit~es used for each subject were deterl~~l?ed by a psychophysical procedure involving six flicker photometric measurements, three under light-adapted conditions and three under dark-adapted conditions. The purpose of the psychophysical procedure was to create a color pair which would be metameric for the rods when isoluminant for the cones. The benefits and method fog creating such color pairs are described in a previous study (Young & Teller. 199 I ). The pupillary responses were obtained in several 3-hr sessions over a period of several weeks. To control possible order effects such as habituation and fatigue. the stimulus conditions were presented in a pseudorandom schedule. Each condition was replicated 30 times. A stimulus trial consisted of an initial delay period of about 450 msec and a temporal change in either the color and/or luminance of the field for about 6 set, followed by a change back to the original field. The long stimulus duration ensured that transient and sustained pupil responses could be differentiated. The pupil diameter was recorded as a function ot’ time using an 80386 computer. The data sampling rate was 60 Hz. Data from each stimulus trial was stored on disk. The averaged response waveform and confidence

PUPIL RESPONSE TO LUMINANCE

intervals were computed off-line after the entire experiment was completed. Digital output from the pupil tracking system was calibrated with artificial pupils of known diameters placed in the plane of the subject’s pupil. The digital resolution of the system was about 32 pm. Component analysis Principal component analysis (PCA), a multivariate technique (Donchin & Heffley, 1978; Heynen & van Norren, 1985), provides one approach to examining the fundamental constituents of the pupil response. In PCA each response waveform is treated as a linear sum of individual components, that is, an amount, ai,, of the F, component added to an amount, a,2, of the F2 component and so on. In general, the waveform Ri of a response evoked by the ith stimulus is, &(t)

= ail .F,(t) + aiz.Fl(t) + . . . + aik.Fk(t)

[Fdm)lFdn)I.&(n).

(2)

The slope, [F,(m)/F,(n)], describes how the amplitude at one point in time is related to the amplitude at other points in time which, in essence, is the shape of the component waveform. If the responses originate from multiple processes, the covariance relationships will not necessarily be linear. For example, for two processes, the covariance relationship is, &(m) = R,(n). ([a;, .F,(m) +

aiz.F,(m)ll[ai,.F,(n) + ~.f’dn)l).

439

type for example, seems to saturate to relatively small luminance changes, whereas others, such as tonic color opponent, generally do not (e.g. Schiller 8c Colby, 1983). Therefore, if the response of a system originates from these two types of visual neurons, one might expect that over the luminance range where the phasic neurons saturate the covariance relationship will be associated mainly with the responses of the tonic neurons. Over this luminance range, the covariance relationship should be linear. The slope of the linear relationship at each latency provides an estimate of (a scalable) waveform for the tonic component. Once obtained, the amplitudes for the tonic component can then be derived by scaling the component waveform in accordance with the steady-state amplitude of each response. The phasic component is derived by subtracting the scaled tonic component from each pupil response.

(1)

where t is time and k is the number of constituent components. Implicit in the equation are the assumptions that individual components do not interact and that the shape and latency of each component does not change. To gain information about the number and shape of the components, the patterns of covariation are examined among time points within a response. If the responses originate from a single process, the covariance relationship will always be linear, because independent of the stimulus condition, the amplitude at one time, m, is always proportional to the amplitude at some other time, n; that is, R,(m) =

AND COLOR

(3)

One can appreciate that R,(m) will be linearly related to R,(n) when ai, = k .aj2; that is, when components 1 and 2 are highly correlated across different stimulus conditions. But for the more general circumstance, when the two components vary independently of one another, the covariance relationship will not be linear. Thus, nonlinearity in the covariance relationship provides evidence that the response originates from multiple processes. The method for recovering the shape of the individual components when there is more than one component generally requires a substantial amount of computation. But there are physiologically plausible circumstances which provide interesting exceptions. The response amplitude of some visual neurons, the phasic broad-band

RESULTS Representative averaged pupil responses to heterochromatic and achromatic luminance exchanges are illustrated for the different subjects in Fig. l(a, b). The column of numbers designates the relative log luminance of the two colors. The number 0.0 indicates that the two colors are isoluminant, as defined by a minimum sustained pupil amplitude criterion (e.g. Alpern & Campbell, 1962). (For the achromatic exchanges, the specification of isoluminance is straightforward. However, for heterochromatic color changes, the specification raises the question of whether luminance should be equated on the basis of a perceptual or a pupil response criterion. As it turns out, the difference between the two is not great. For subjects A, C, D, and E, the relative luminance for a minimum sustained pupil amplitude is very close to the isoluminant level determined psychophysically. For subject B, color 2 is -0.10 log units dimmer than color 1 when equated using the minimal sustained pupil amplitude criterion compared to the perceptual criterion.) The comparison (Fig. 1) between pupillary responses evoked by heterochromatic and achromatic luminance increments reveals that the responses to the achromatic and heterochromatic stimuli are nearly identical when the luminance is incremented by 0.10 log units or more. The results for all subjects are similar with the possible exceptions that at the highest luminance increment the heterochromatic response is slightly greater than the achromatic response in subject B, whereas the reverse is found in subject D. The resting pupil diameter just prior to the stimulus onset was, on the average, 5.7 mm (ranging 4.065 mm) for the five subjects. The amplitude of the pupil constriction to a 0.10 increment was 1 mm or less. Pupil responses to very small, achromatic luminance increments (Fig. 2) were also obtained during the same experiment described in Fig. 1. The results document that for achromatic luminance increments < 0.30 log units the pupil responds in a purely-transient fashion. The transient response, however, only occurs after the onset of the increment. The pupil diameter returns to its

440

ROCKEFELLER

resting diameter even though the stimulus luminance remains incremented. This findinn occurs in all five subjects tested.

SUBJECT A

S. L. YOUNG r/t a!.

We used PCA to gain insights about the compositw of the pupil response waveform. Figure 3 illustrate< the ..covariance in the pupil amplitudes at two representative

SUBJECT B

SlBJECT C

J;;-------“‘ :;#;;y /’

v color 11

color 2

I

color 1

color 2

SlJBJ&CT0 -0.25

W

I

1 color 1

color 2

1

color 1

SUBJECT E

.__) r__,.._.___._..--.-_...v-.

_.

TIUE

(2s)

^_ _. _

-0.10

xt/ ../---_---_-----

+0.25

w

+0.30

color1 1

wlor 2

I

cotorl

I

color 2

j

color I

FIGURE 1. Pupii responses to achromatic (dashed waveforms) and heterochromatic (solid waveforms) luminance exchanges of spatially homogeneous stimulus fields. In the achromatic condition, color 1 and color 2 were both white. In the heterochromatic condition, color 1 was purplish and color 2 was white. Representative responses of five subjects are shown. The luminances, however, were incremented by different amounts for subjects A--C (a) and subjects D-E (b). The vertical column of numbers designates the relative log luminance increment. The number 0.0 designates the approximate isoluminant level as determined by a minimum sustained amplitude criterion.

PUPIL RESPONSE TO LUMINANCE

441

AND COLOR

SUBJECT A

SUBJECT B

SUBJECT D

SUBJECT E

TlME (26)

SUBJECT C

FIGURE

2. Pupil responses to small luminance increments. For luminance increments aO.30 log contrast units, the pupil response is sustained. For smaller luminance increments, the pupil response is purely transient.

can account for the variance in the pupillary responses. The template of a sustained component waveform for the achromatic condition was recovered from the slopes of the upper portion of the covariance relationship (Fig. 3, bottom). Each amplitude waveform (Fig. 4, middle column) was then derived by scaling the template at each point in time with respect to the steady-state amplitude of the pupillary response. The existence of an additional component (Fig. 4, right column) is inferred from the substantial difference between the original response (Fig. 4, left column) and the sustained component (Fig. 4, middle column). The observation that the shape of the residual responses changes only little as a function of stimulus luminance suggests that a single component accounts for the variability in the residual responses. From the template of the sustained

latencies. If the pupillary responses were mediated by a single linear process then these (and any other) covariante relationships would all be linear. However, the pupil amplitudes for latencies corresponding to the peak of the pupil constriction generally varied nonlinearly with the amplitude at later latencies in the pupil response (Fig. 3, bottom). Thus, the analysis suggests that either the pupillary response is mediated by multiple linear processes or by a nonlinear process (e.g. a process in which the response waveform or latency changes substantially with luminance increments). It is important to appreciate that PCA does not necessarily uncover the physiologically best-fit component waveforms. But the analysis can demonstrate how well candidate processes such as one with a purely transient waveform and one with a sustained waveform

a

-,

0

1

2 -1

0

1

2 -1

FIGURE 3. Representative patterns of covariance covariance relationship is linear over a certain range corresponding to the peak of the pupil constriction indicates that the pupil response

0

1

SubjectE

SubjectD

SubjectC

SubjectB

SubjectA

2

-1

0

1

2

-1

0

1

Amplitude (mm) 0 4.78s in the pupil response to achromatic luminance increments. Although the of latencies (top), the covariance relationship is nonlinear over the latencies (bottom). In accordance with PCA, the nonlinear covariance relationship waveform is composed of more than one component.

ROCKEFELLER

442

component waveform derived for the achromatic luminance condition, the sustained (Fig. 5, middle column) and transient (Fig. 5, right column) amplitude waveforms for the heterochromatic stimulus condition were also derived. The main insight gained by this demonstration (Figs 4 and 5) is that the composition of the pupillary responses evoked by the heterochromatic and achromatic luminance increments is not very different. Responses evoked by either condition can be described quite well as a linear sum of the same two components. In order for PCA to detect the existence of separable components, the stimulus-response property of these components must correlate poorly with each other. A plot of the amplitudes as a function of the luminance increments (Fig. 6) illustrates the stimulus-response functions for the derived transient and sustained components. The exact stimulus-response properties revealed by the analysis depends on where the experimenter locates the intersection of the upper and lower branches of the covariance function. For the covariance functions shown at the bottom of Fig. 3, the amplitude of the transient component saturates at very small luminance increments (Fig. 6, top), whereas the ampli-

Response

C L. YOUN(;

Pf Cl/

rude of the sustained portion of lhe respo~r~ IIIC~CXSC:~ monotonically with the stimulus luminance rncremenl (Fig. 6, bottom). The transient component amplitudr saturates regardless of whether the stimulus 1s ;III achr~~~ matic or heterochromatic change, the maximum amplitude obtained

almost

the same for both ccondition>

DISCUSSION

The possibility that the pupillary reflex is mediated by separate processes (one responsive to luminance and one responsive to color) was suggested by previous observations that the steady-state diameter of the pupil varies systematically with luminance levels independently of the stimulus color while a purely transient constriction is evoked by isoluminant color changes. However. if one portion of the pupil response is evoked by color and another portion evoked by luminance changes, the two portions of the response should summate when the eye is stimulated by a heterochromatic luminance increment (or the response evoked by the heterochromatic stimuli should at least be larger than that evoked by the achromatic stimuli). Our results (Fig. I) show that while a substantial response is evoked by either isoluminant

Sustained Component

Transient Component

Subject A

Subject B

Subject C

Subject D

Subject E

FIGURE 4. The original responses (left column) from the achromatic luminance experiments and their derived PC4 components. The shape of the sustained component (middle column) was derived by analyzing the slope of the upper limb of the covariance relationship shown in Fig. 3. The transient component (right column) is the difference between the original response and the derived sustained component. The transient component responds only at the onset of the achromatic luminance increment. The results of the component analysis illustrate that the pupil response can be described quite well a~ a linear sum of a sustained and a transient component.

PUPIL RESPONSE TO LUMINANCE

color exchanges or by achromatic luminance increments the pupillary responses evoked by a color change with a luminance increment are generally identical to those evoked by a luminance increment alone. Only over a small range of luminance increments near the isoluminant level do the responses evoked by heterochromatic and achromatic stimuli differ appreciably. This finding is relevant to our understanding of the nature of visual input as the finding cannot be easily dismissed by postulating a saturation of the iris muscle contracture. With an average resting pupil diameter of 5.7 mm and a typical constriction of 1 mm, the pupil diameter is still considerably larger than the expected minimum diameter or 2 mm. Additionally, in two subjects examined, we found that the pupil could constrict further when the eye was stimulated with 0.54.7 log luminance increments. If the pupillary reflex is mediated by separate processes that can sense luminance or color, then we would also expect the composition of the responses to heterochromatic and achromatic stimuli to differ substantially. Because heterochromatic luminance exchanges produce both a luminance and color change, one would expect the response to be more complex than that

Response

AND COLOR

443

produced by an achromatic luminance exchange. But PCA does not provide support for this expectation. Our results show that both the number and the waveform of the response components for the heterochromatic and achromatic conditions are similar (Figs 4 and 5). We therefore conclude that there is no obvious evidence that pupillary responses are mediated by separate, luminance- and color-specific visual pathways. The present results, however, support the idea that visual input to the pupillomotor system is organized into phasic and tonic pathways. Results from our PCA demonstrate that the pupillary responses can be described as a linear sum of two components, one with a sustained and one with a transient waveform. Furthermore, the stimulus-response properties of the transient component are similar to those reported for certain phasic broad-band neurons in primates. Similar to the finding that some phasic broad-band neurons respond to isoluminant color as well as achromatic luminance changes (e.g. Schiller & Colby, 1983; Derrington, Krauskopf & Lennie, 1984; Lee, Pokorny, Smith, Martin & Valberg, 1990), the transient pupil component also responds to both color and luminance changes (Figs 1,2,4 and 5). Phasic broad-band neurons respond

Sustained Component

Transient Component

Subject A ~=Q=-~V

Subject B

Subject C

Subject D

Subject E

FIGURE 5. The original responses (left column) from the heterochromatic luminance experiment and their derived components. The sustained component (middle column) was derived using the same sustained waveform shown in Fig. 4. The transient component (right column) is the difference between the original response and the derived sustained component. The transient component responds to either direction of the color change. These results again illustrate that the pupil response tail be described quite well as a linear sum of a sustained and a transient component.

444

ROCKEFELLER

S. L. YOUNG

Subject D

Subject C

Subject 13

Subject A

VI crl

-y----l

__

i 5

-1

0

1

-1

0

1

-1 Log

0 luminance

1

-1

0

1

-1

n

increment

FIGURE 6. The peak amplitudes of the transient (top) and sustained (bottom) components illustrated in Figs 4 and 5. The amplitudes are shown separately for the achromatic (open square) and heterochromatic (large, solid triangle) luminance increments. The achromatic and heterochromatic luminances were equated on the basis of the sustained pupil amplitude. The two sustained curves (bottom) were shifted horizontally for best fit (by eye); the two transient curves (top) were shifted horizontally by the same amount. Additional transient amplitude data (small, solid triangle) are included to show that the pupil still exhibited a transient constriction to the heterochromatic exchange when the luminance was decremented by 0.2 or less log contrast units.

differently to luminance and color changes; they respond only once to each cycle of a spatially-homogeneous luminance change (i.e. either to the onset or the offset, but not both) and twice to each cycle of color change (i.e. to both directions of the color change). The transient pupil response component behaves similarly (Figs 4 and 5). Similar to the finding that the response amplitude of these neurons becomes balanced when the colors in a color exchange are perceptually isoluminant (e.g. Schiller & Colby, 1983; Lee, Martin & Valberg, 1989) the amplitude of the transient pupil response also becomes balanced near isoluminance [Fig. l(a, b)]. Some investigators concluded that in monkeys phasic and tonic visual neurons can be distinguished by their contrast gains. Specifically, the phasic broad-band neurons have a relatively high achromatic contrast gain to stimuli around the steady-state adaptation level and their responses saturate as a function of increasing luminance increments (e.g. Shapley, Kaplan & Soodak, 198 1; Kaplan & Shapley, 1986; Purpura, Kaplan & Shapley, 1988). Our results suggest that the transient upil response component has similar gain characterXit ,s .t6 these phasic broad-band neurons. The finding $.trely transient pupil component is evoked by a luminance increment (Fig. 2) suggests that the ent has a relatively high contrast gain. Results

from the PCA suggest that the amplitude of the transient component saturates at higher luminance increments (Fig. 6). Pupil studies in subprimate species have elucidated the role of tonic visual neurons as inputs for the pupillomotor nucleus. The sustained aspect of the pupillary response in rats is mediated by tonic visual neurons (e.g. Trejo & Cicerone, 1984; Clarke & Ikeda, 1985a, b). Tonic-on type neurons mediate pupillary constriction. whereas tonic-off type neurons (much fewer in number) mediate pupillary dilation. In cats, tonic-on W-cells seem to be the most likely visual input for pupilloconstrictor nuclei (Stone & Fukuda, 1974). The type of visual neurons controlling the sustained aspect of the pupil response in monkeys or in humans remains to be identified. An alternative explanation to the phasic-tonic visual neuron hypothesis is that the transiency and sustenance of pupillary responses arises from some nonlinearity in the motor pathway. Sun and Stark (1983) advanced the idea that the shape of the pupillary response waveform evoked by stimulus changes is influenced by the resting diameter of the pupil. Controlling the resting pupil diameter by varying the accommodation level, they showed that large pupil diameters (6.9.-8.0 mm) promote response transiency (pupillary escape), whereas small pupil diameters (4.0.-5.0 mm) promote response

PUPIL RESPONSE TO LUMINANCE

sustenance (pupillary capture). Their idea provides one explanation for the transient pupil constrictions observed under scotopic illumination levels (e.g. Lowenstein & Loewenfeld, 1969; Sun, Liu & Liu, 1981). But, as the present results show, a purely transient constriction can be evoked by isoluminant color exchanges or by small luminance increments even at photopic levels where the subjects’ pupil diameters were much smaller than the 6.9-8.0 mm range; in some of our subjects, pupil diameters even lay in the 4.G5.0 mm range. Thus, we adhere to the notion that the occurrence of a purely transient constriction is related more to the nature of the visual stimulus than to the resting diameter of the pupil. In conclusion, the present results support the idea that the visual input to the pupillomotor nuclei in humans is organized into phasic and tonic pathways. These results also suggest that the phasic pathway to the pretectum has stimulus-response properties similar to the phasic pathway to the lateral geniculate nucleus.

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<‘I
Ac~kno~rledgm~mts~~~I’l~~s work was supported by .\aliiiiidl $.!c liib!i tute Grants (EY07913 and EY08384) to R. S. L.. Luirng .tnd h> isi, unrestricted grant from Research to Prebcnt Blindr~w. lrti I?) Ihi Department of Ophthalmology and Visual Sciences. R:>hrr! Shaplc!. Randy Kardon. and Eiji Kimura provided valuables C(mm~:nt\ ‘>:I Llfj earlier draft of this paper