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Afterimage and pupillary activity following strong light exposure
v&h
Res. Vol. II. pp. 275-288.PorgamonRes
AFTERIMAGE
1971.Printedin Grut
Britain.
AND PUPILLARY ACTIVITY FOLLOWING STRONG LIGHT EXPOSURE DAVID A. NEWSOME
Ophthalmology Branch, National Eye Institute, National Institutes of Health, U.S. Department of Health Education, and Welfare, Bethesda, Maryland 20014, U.S.A. (Received 30 April 1970; in revised form 29 June 1970)
INTRODUCTION PUPILLARY behavior in darkness after exposure to pre-adapting luminances of weak or
moderate intensity has been measured (REEWS,1918; YOUNGand B~nrsw~~, 1954), but activity following extremely bright light has received little attention. ALPERN and CAMPBELL (1963) reported that, after 3 min adaptation to intense light, the pupils in darkness first dilated and then reconstricted. They interpreted their findings as showing that the retina under these conditions continued to activate the pupil in the absence of external stimuli. A re-examination of this phenomenon was undertaken, using a method that allows continuous recording of pupil size in darkness. The results in this report confirm Alpem and Campbell’s findings; in addition, some previously undescribed aspects of pupillary activity after strong light exposure and their intimate association with afterimages are presented. METHODS Nine normal young adults participated. Detailed observations were made on six of these. Pupillary activity was recorded continuously by the electronic infrared pupillograph of LG~ and LOEWENFELD (1958). The subjects sat in a dark room withchii and forehead supported, and their eyes shielded from the stray light of the instrument. After 10-15 min dark adaptation, the subjects occluded the right eye and tixed with the left on the center of a 17 x 20’ quadrangle of about 3-5 x lo6 trolands brightness. The intensity of this light was measured to be about 10 log units above scotopic visual threshold (see Fig. 1). The standard light stimulus consisted of a 2-min exposure to this iield. As soon as the light was turned off, recording of pupil sire was begun. Pupillary movements were recorded continuously for 10-15 min; thereafter, 15-30 set long tracings were made at l-min intervals up to 30 min in darkness. In most sessions no fixation light was used; the subjects maintained steady gaxe with no reported ditliculty. When used, the fixation point was 5 mm/dim red spot, l-m distant, viewed via the front surface mirror of the pupillograph. One-minute and longer exposutes to the bright adapting light were separated by at least 24 hr; with short (30 set or less) or less intense light stimuli, about 1 hr was interposed between exposures. Intensity of the light stimuli was varied with Wratten neutral density filters, and stimulus duration by a hand switch and stop watch.The subjects controlled an event marker on the pupillograph tracing by a hand switch. They were instructed to mark the record (1) when the positive afterimage began to appear, (2) whenever it became brighter, and (3) when it could no longer be seen. The negative afterimage was observed against a field of about O-4log ft-L uniform surface illuminance located 8 ft from the subjects. The ‘end-point” for the negative afterimage came when it could no longer be seen against this background illumination. Condensed tracings of pupil activity were made from the original records by sampling pupil size at 1-set intervals. Since the responses of the stimulated and consensually reacting pupils were equal in all experiments, the trace of only one pupil is shown in the figures. In other experiments pupil activity in a steady dim light was tested. Dark-adaptation time and experimental set-up were unchanged (see Fig. 1) except that the voltage to the stimulator lamp was reduced with a Powerstat so that the field brightness matched approximately the peak intensity of the afterimage. This matching was done by the subjects in preliminary experiments. 275
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EXPERIMENTAL
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Fro. 1. Bperimental set-up. As the subject sat in darkness, his left eye was e%po& to a 17 x 2tY *Id of about 3-5 x lo6 trolands brightness, after which pupil movements in darkness were
recorded by an electronic i~m-~-~siti~
scanning device.
RESULTS
(1) Pupil actiuify Figure 2 shows the behavior of one subject’s pupils in darkness after a Zmin exposure to the ftil intensity of the adapting Iight. When the light was extinguished, the pupils began to dilate smoothly and rapidly. This dilation had a brief latent period that could not be measured precisely for technical reasons, but was shorter than 0.5 sec. The dilation was I INITIAL
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Fro. 2. Pupil activity in darkness (Subject MH). After a 2-n& exposure to the stimulus light (“light off’ at arrow), the pupils first dilated rapidly, then reconstricted and showed unrest for about 5.5 min. Thereafter the constriction diminished gradualiy and quietly until fully darkadapted sire was reached. The pupils then remained quiet to the end of the experiment. The positive afterimage was first seen after 6 set darkness; the first small arrow shows when it reached maximum brightness, the second when it disappeared, and the thiid when the negative afterimage could no longer be seen.
2n
Afterimage and Pupillary Activity following Strong Light Exposure
but, before the pupils reached dark-adapted sire, they recontracted. This recontraction was not smooth. Rather, it took the form of low-frequency pupillary unrest with swings of large amplitude. The reconstriction with unrest gradually lessened, then disappeared rapidly after 45-6 min, depending on the subject. A phase of gradually diminishing constriction without unrest followed, and, about 15-18 min after “light ofI”, full pupil size was reached. Similar behavior was found in all subjects’ pupils, but details of amplitude and frequency of the oscillations varied among individuals (see Fig. 3). Only one of the nine subjects (DL, see Fig. 4) had an average amplitude of recontraction less than 2 mm (as measured from dark-adapted pupil sire); her pupils recontracted slightly more than 1 mm. For this group of subjects, pupil size at the end of the light exposure was usually about 3 mm, with initial dilation to 6-8 mm. The average diameters at maximum reconstriction ranged between 45-6 mm, and at full dark adaptation between 7-8-5 mm. extensive,
(2) Visualphenomena When the 2-min bright light stimulus was turned off, none of the subjects saw an afterimage immediately. After several seconds of complete darkness a positive afterimage TT Positive
After-image
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Fro. 3. Four subjects’ pupil activity in darkness after 2 min full-intensity light. These curves show inter-personal variations in (1) average amplitude of recontraction, (2) duration and amplitude of unrest, and (3) the correspondence between duration of recontraction with unrest and duration of the positive afterimage (shown by the bar above each curve).
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DAVID A. N~wsom
appeared. It grew brighter, peaked, and passed through a series of dimmings and brighten-
ings before gradually fading away. The appearance of the positive af&image cointided with the ~n~~ of the ‘pupillary ~~~~on in darkness- Fading of the a&image was accompanied by the gradual decrease in the amplitude of the pupillary unrest, aud its full disappearance with the beginning of the quiet phase of diminishing constriction toward fully dark-adapted size (see Fig. 2). All subjects were asked to indicate with the event marker whenever the afterimage brightened. This subjective sensation of brightening usually Cain&led almost perfectly with the more marked ~on~~tio~~ of the pupillazy unrest (see Fig. 4)*
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When the positive afterimage had disappeared permanently, the presence of the negative afterimage was followed until it could no longer be seen against the dim iudu~~~~ field. After a full-int~~~ty Z-min light exposure, six subjects could see a negative afterimage for an average of 24-1tin after “fight 0iP (from 224&S min). 1n each case the negative afterimage persisted several minutes after full pupil size in darkness had been reached. (3) Stimulus intensity
The presence and degree of recontraction of the pupils after initial diiation at ““fightoff” depended on the intensi~ and duration of the preceding light stimulus. When stimulus duration was held constant at 2 min while the stimulus in~nsi~ was decreased, duration and amplitude of the following pupillary recontraction with unrest decreased progressively (see Fig. SB, C). When the light intensity had been reduced 2 log units (Fig. 5D), the pupils dilated steadily and rather rapidly to full size without showing recontraction or unrest, even though
Ma-image
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Fm. 5. Effkct of clcm&ng intu&ty of light stimuh~~. 7% same subject was given four 2-e tight stimuli, with the brightncnsprogmssively diminished fmm fti intensity (A). The period of pupikry recontraction with unrest was progressively diminished when the lit was reduced by O-6 log units (II), and l-6 log units Q; it was absent when a 2-Olog filta: was
interposed (D). With the weakest light them was no latent period for the positive afterimage.
the afterimage did (subjectively) fluctuate in brightness. With this reduced stimulus intensity there was no latent period for the positive ~te~rna~. (4) Stimulus duration Papillary activity and afterimage phenomena varied also when the intensity of the preceding light stimulw was held constant and its duration changed. With fidl stimulus intensity and exposure times shortened progressively, the period of recons~ction with unrest became shorter, and disappeared entirely with stimuli shorter than 1 set (see Fig. 6). When the subjects were shown the bright light stimulus for only 0.5 set, all saw the afterimage immediately at “light off”. The minimum light exposure required to produce a latent period before the appearance of the positive afterimage varied from subject to subject, ranging between 1 and 5 sec. The duration of the latent period increased with the duration of the preceding light, reaching a plateau after 2 min exposures (Fig. 7). (5) Pupillary activity after brief light stimuli With bright light stimuli of 1 set or less the pupil behaved differently than with longer
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FIG. 6. Effect of decreasing duration of the light stimulus. The same subject was given the full intensity light stimulus for exposures up to 4 min (D). Decreasing the duration of exposure to 1 min (c) and then to 10 set (B) shortened the length of the afterimage latent period, lowered the peak of the initial pupil dilation, and diminishedthe extent and duration of the rccontraction with unrest. When the Hposure was for only 1 set (A), the afterimage was seen immediately, and pupillary recontraction was absent.
stimuli: at the end of the light exposure it remained contracted for a few seconds before dilating with little or no unrest and no recontraction phase (see Fig. 8). In addition, the afterimage latent period was missing after’such short, high intensity light stimuli. (6) Retinal hypoxia Two subjects produced what was presumed to be transient hypoxia of the retina by exerting finger pressure on the Fre-exposed left globe. When this was done, the pupils dilated. When pressure was released and the afterimage reappeared simultaneously the pupils again contracted (see Fig. 9). Pressure on the non-stimulated right eye did not afkt pupil size. (7) Pupillary oscillations in dim steady light In two subjects the left eye was exposed to the same stimulus field as already described, except that the light intensity was dimmed to a level matched as closely as possible to the
Afterimage and Pupillary Activity following Strong Light Exposure
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Fro. 7. Infiuence of duration of light stimulus on latent period of afterimage. (Pour different subjects, full light intensity.) With ail other parameters constant, the stimulus duration was lengthened from 0.5 set to 4 min. Stimulus time above 2 min produced little further increase in latency of the positive afterimage.
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FIG. 8. Prolonged pupil contraction after brief flash of intense light (subject RB). After a 05 set flash of light about 10 logs above scotopic visual threshold (. . . . . .) the pupillary contraction lasted much longer than that elicited by an equally long but less intense light flash about 75 logs above threshold). In both cases the positive afterimage was seen (-, immediately.
peak intensity of the afterimage (see Methods). In the presence of this steady, dim light the pupils showed unrest resembling closely that observed in the afterimage experiments. The similarity of the same individual’s unrest under these two different conditions, and variations between subjects, are illustrated by the frequency analysis for pupil oscillations of different amplitudes shown in Fig. 10.
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DAMD A. Nawso~e
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FIG. 9, Effect of retinal hypoxia on Pupillary recontraction after exposure to bright light. During the period of recontraction in darkness (75-100 set after 2-min bright light stimulus) the subject pressed firmly on the stimulated eye (OS, 0 C?0 01, or on the unstimutated eye (OD, * *a e,2. when the retina of the stirdated eyewasmade iscbemic in this way the aftarimage disappeared and the pup% dilated; they reconstricted when pressure was r&a& (arrow, “‘OFF”]. When the unstimulatedeye wascompressed,the pupils remained contracted.
DISCIJSSION Under the conditions used in these experiments, pupillary activity following very bright light stimtii showed three distinct phases: (1) an initial pupillary dilation, lasting several seconds, (2) marked pupillary reconstri~io~ with unrest, beginning with the appearance of the positive afterimage and lasting between 4.5 and 6 min, and (3) a final phase of quietly diminishing contraction lasting 8-12 min and ending when full dark-adapted pupil diameter was reached, before the disappearance of the negative afterimage. In this sequence of events three main phenomena appear to play a role. These will be discussed separately.
The pupiIlary reconstriction observed in these experiments was extensive and long-lasting, What is the source of this activity? It could be thought that the constriction was produced as the subjects accommodated on the positive afterimage when it appeared. However, the pupils reacted the same when the subjects looked at a far fixation spot during the test and when they did not. Furthermore, pupiftary re~ntra~ion occurred only after iight stimuli 940 log units above scotopic visual threshold. A diminution of stimulus intensity by 2 logs abolished the recontraction phase and the pupils dilated smoothly and quickly, even though a positive afterimage was seen.
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Afterimage and Pupillary Activity following Strong Light Exposure
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FIG. 10. Frcqmmcy pattern of pupiihuy oscillations under two different experimental conditions (two subjazts). In each experiment the amplitude of all individual pupil oscillations The ordinate shows the number of pupil o6mmingwithina130aactimapcriodwasoscillations and the abscitm amplitude of them ~WJ (ii O-l-mm units). The intensity of the steady dim light was matched ~p1clo~ly~m_~lc to the peak brightness of the positive .
Fatigue can produce extensive pupillary oscillations (LOWJSNSTEIN, FEINBERG and LOE1963), but in normal subjects these are not seen so soon after the beginning of the experiment, and since the pupils eventually became large and quiet after dark adaptation, the subjects were undoubtedly alert. The timing of the initial phase of marked pupillary contraction (456 min) and of the following phase of gradually diminishing contraction (8-12 min) suggests that the first contraction phase may be related to cone function, and the following phase to rod function. The coincidence of the positive afterimage with the first recontraction phase, and of the subjective negative afterimage with the phase of diminishing contraction supports this view. To test the dependence of the pupillary constriction on cone function, two persons with rod achromatopsia were examined using the full stimulus intensity for 2 min (see Fig. 11). The period of recontraction with unrest was absent entirely in one of them (GE) and markedly attenuated in the other (DM). This latter observation is consistent with the fact that DM had a few functioning cones (G~URQ and GUNKEL,1964). With shortening exposure to the stimulus light, DM’s pupils-just as those of the normal subjects-took less time to reach full diameter. Both the subjects with rod achromatopsia saw amorphous, short-lived afterimages compared to the sharply etched images described by the normal subjects. DM’s drawing of what she saw, along with what a normal individual drew, is shown in Fig. 12. Cone function appears, then, necessary to the phenomenon of marked pupillary recontraction after exposure to very bright light. The rods-probably responsible for the second WDIFELD,
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Flo. 11, Pupil&y movements after bright light exposure in persons with rod achromatopsia (two subjects). The upper curve shows the movemcuts of GE’s pupils after a 2-min exposure to the bright adapting light. Note the absence of reconstriction with unrest, and the comparatively brief duration of the positive afterimage. The tower three curves show the nsponsas of DM’s pupils after progressively longer full-intensity light stimuli. After the 2-min exposure to full stimulus intensity (. . . . . .) there was a small amount of re~onstriction.The differenceain final pupiIs sizes for this subject is explained by the fact that the experiments were run on separate days.
phase of dim~shing contraction-ap~r to be mu& less effective in activating the pupil under these conditions than are the cones. This assumption fits well with the characteristics of pupiflary reactions elicited via the rods in other experiments: while the pupi~omotor threshold of the retinal periphery is much lower than that of the fovea (particularly when blue light is used), its motor efficiency is quite low (see, LOWENFELD,1966, Summary).
The latent period for the appearance of the positive afterimage, accompanied by fast pupilllary dilation during the first seconds in darkness, reflects an absence of afferent (visual and pupillary) stimulation immediately after prolonged exposure of the retina to powerful light. Such an absence of retinal discharges could be due to photochemical mechanisms (compare BRINDLEY,1962) or to neural influences, that is, temporary cessation of conduction by retinal neurones, In other words, the threshold for pupillary (and subjective visual) responsiveness may have been raised so high by the intense retinal stimulation (or bleaching)
Afterimage and Pupillary Activity following Strong Light Exposure
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FIQ. 12. Afterimage of normal subject and of one with rod achromatopsia. After a 2411 exposure to the 17 x 20” field at brightness, normal subjects reported seeing a sharply outlined, lemon colored afterimage with a contrasting magenta halo, as shown on the left. Under the same conditions a subject with rod achromatopsia saw the “fuzzy” afterimage which was drawn as shown on the right. The subject saw no color.
that the system fails to respond to the relatively low intensity of the afterimage activity until some retinal dark adaptation has taken place. That such an inability to respond to weak stimuli really exists is shown by the following experiment. One of the subject’s eyes was exposed for 2 min to the full-intensity stimulating light. When the afterimage appeared after “light off”, the subject matched as closely as possible the intensity of the stimulus field (reduced by rheostat) to the peak brightness of the positive afterimage. In subsequent experiments the eye was again stimulated for 2 min at full intensity. Beginning 1 set after “light off”, the previously matched light was presented during the period of initial rapid pupillary dilation. This stimulus was not seen, and did not affect the pupil until about 0.5 set after the positive afterimage appeared. The afterimage latent period and the coincident rapid pupillary dilation depended on the total energy of the adapting light. As full stimulus intensity was reduced, or as the light was shortened, the latent period for the afterimage and the peak of the initial dilation were reduced. In fact, with very short full intensity stimuli the pupillary constriction outlasted the stimulus up to several seconds, and the full brightness of the afterimage was seen immediately at “light off”. In view of the relatively short duration of the afterimage latent period with pupillary dilation it appears likely that these phenomena are caused by cessation of neural conduction rather than by a sudden interruption of the relatively long lasting photochemical process. The afterimage also disappeared and the pupil dilated when blood flow to the eye was impeded by pressure. This similar phenomenon is known to be caused by loss of conductivity of the neural elements due to hypoxia of the retina. A number of authors have described retinal damage in animals by visible and invisible light energy (NOELL, WALKER, KANG and BERMAN,1966; KUWABARA and GORN, 1968) and recently DAWSON and HERRON (1970) showed that in normal human subjects prolonged exposure to the full intensity of an indirect ophthalmoscope raised dark adaptation thresholds during the first 8 min after exposure. Dawson and Herron pointed out that a large amount of infra-red radiation is produced by tungsten sources such as the ophthalmoscope lamp. Since our light source was also tungsten, it seemed of interest whether an intense adapting light with very little infra-red energy would also produce the afterimage latency phenomena. A Grass
Dc;vn, A. Ntwsom
286
photic stimulator was used, via an infra-red reflection titer (100 &she&z, flash duration S-msec, intensity 9.3 log units above scotopic visual threshold). Following 2 min adapting exposures to this light, more than 3 set elapsed before the afterimage could be seen. (3) Oscillatory behavior During the first, marked recontraction period both the pupils and the afterimages showed fluctuations that usually coincided. It therefore appears reasonable to assume that the retina is the source of these fluctuations. Each subject had a distinct pattern of oscillations repeatable in successive tests; and for each person a similar pattern of pupillary unrest was recorded in the presence of steady, dim light of an intensity matched approximately to the brightness of the afterimage. Under these conditions the subjective visual sensation did not fluctuate, and yet the pupil did. While we cannot explain why there is similar pupillary activity in the absence of subjective (visual) fluctuations, such pupillary oscillations in the presence of steady illumination are well known, and have played a considerable role in the clinical literature under the names of “pupillary unrest”, or, if marked, “hippus” (see 1969, Summary). The rate and amplitude of such lightL~WENST~N and LOW, induced pupil unrest depend primarily upon the intensity of the illumination and secondarily upon personal characteristics, that is, unrest tends to be most ample in young, excitable individuals. The particular pattern of oscillations for each individual is determined by genetic factors as shown by the fact that the pattern is the same in identical twins (see Fig. 13).
LIGHT
INTENSITY,
log,o
units
Fro. 13. Patternof pupil oscillations in five normal subjects under influence of lights of varying intensity.1 The ordinate represents the average amplitude of each subject’s pupil oscillations occurring within a 2OO-secperiod for each light intensity step marked on the abscissa. (23 Year old men; (. . . . . .), 25 year old man; (- - - -), 21 year old woman. u. W), dak from identical (monozygotic) 23 year old male twins. Note that the amplitude protile diikr considerably among the unrelated subjects. These profiles were found consistently for each individual in repeated tests. Between the identical twins the values were as similar as were two successive exp&ments in the same individual. 1 Unpublished experiments (I. E. bJEWENFELD ) from the Lowenstein Laboratory of Pupillmphy, Columbia University, College of Physicians and Surgeons, Department of Ophthalmology.
Afterimageand Pupillary Activity followingStrong Light Exposure
287
This light-induced pupillary Unrest is assumed to be elicited by afkrent stimuli at a central nervous site, probably the oculomotor nucleus (YOUNGand BIERSDORF,1954). The precise mechanism is unknown. Acknowlcdgcmcnts-The author is grateful to Dr. IRENE~F3vENm.D and Dr. Parart Gosuggestions in this study.
for their helpful
SUMMARY Pupillary activity in darkness following exposure to strong bright light was recorded and found to occur in distinct phases, namely, (1) an initial dilation followed by f2) reumtraction of several m&meters with relatively siow, l~~~~tu~ pupillary osciltations for 4.5-6 min, (3) a phase of gradually decreasing contraction without unrest Ming 8-12 min, and (4) stable pupils after full sire was regained. Under these experimental conditions the appearance of a positive afterimage was preceded by a latent period up to 12 sec. The phase of pupillary recontraction with unrest coincided with the appearance of the positive afterimage, and was reduced or absent in patients with rod achromatopsia. The later phase of gradually diminishing contraction ended before disappearance of the negative afterimage and had a time course rdmilar to that for recovery of rod sensitivity after bleaching. Both pupil& and visual phenomena were found to depend on the intensity and duration of the adapting stimulus fight. Similarity of pupilhuy oscillations in the presence of the af&mage and in the presence of an external steady light of similar brightness was shown. The oscihations have not been noted previously. REFERENCES ALPERN, M. and CAMPBELL,F. W. (1963). The behavior of the pupil during dark adaptation. J. Physfof. 165 5-7. I3rmmrx~,G. S. (1962). Two new propertiesof foveaI after-imagesand a photochemical hypothesis to explain them. J. Physiol. 164,168-179. DAWSON, W. W. and Hrmto~, W. L. (1970). Retina1 i&mination during indirect ophthalmoscopy: Subsequent dark adaptation. Zest. Ophthd 9,89-96. GOURAS, P. and GUNKEL,R. D. (1964). The frequency response of normal, rod achromat and nyctalope ERGS to sinusoidal monochromatic light stimulation. Documenfa Opthul. 18,137-1x). KUWABARA, T. and GORN,R. A. (1968). Retinal damage by visible light: An electron microscope study. Arch. Ophthal. 79,69-78. Lo~wzmw,
I. E. (1966). Pupiky rno~~ associated with light and near vision: An exp&menta! review of the literature. In Recent Deocfupments in Vision Research (edited by M. Wmrcam), National Academy of Sciences, National Research Council, Washington, pp. 17-105. ~WENSRSN, 0. and bEwENIm& I. E. (1958). Electronic pupillography. A new imtrumant and some clinical applications. Arch. Ophthul. 59,352-363. ~wEN~~~J, 0. and bEWENF&D, I. E. (1%9). The pupil. In The Eye (edited by H. D~vso~), 2nd Edn., Vol. 2, Academic Press, New York, pp. 276-277. L~WENSJZIH, 0.. FEINISERG, R. S. and L~~EXFEL,D, I. E. (1963). Pupillary movenents during acute and chronic fatigue. Znvest. ~~~t~i. 2,138157. Now, W. K., WALKER,V. S., KANG,B. S. and BF.RMAN, S. (1966). Retinal damage by hght in rats. 1-t.
Ophthal. $450-473. REEVFB,P. (1918). Rate of pupillaty dilation and contraction. Psychol. Reo. X$330-340.
YOUNO,F. A. and BIERSWRF,W. (1954). Pupillary contraction and dilation in light and darkness. J. camp. physiol. Psychol. 47,264-268.
~~-~pi~i~ activity in darkness following exposure to strong bright light was reoorded and found to occur in distinct phases, namely, (1) an initial dilation followed by (2) recontraction of several milliietem with relatively slow, large-amplitude pupillary oscillations for 4.56 min, (3) a phase of gradually decreasing contraction without unrest lasting 8-12 min, and (4) stable pupils after full sire was regained. Under these experimental conditions the appearance of a positive afterimage was preceded by a latent period up to 12 sec. The phase of pupillary recontraction with unrest coincided with the appearance of the positive afterimage, and was reduced or absent in patients with rod achromatopsia. The later phase of gradually finishing contraction ended before disappearance of the negative afterimage and had a time course similar to that for recovery of rod sensitivity after bleaching. Both pupillary and visual phenomena were found to depend on the intensity and duration of the adapting stimuius light. Similarity of pupillary oscillations in the presence of the afterimage and in the presence of an external steady light of similar brightness was shown. Some possible mechanisms for these phenomena are discussed.
DAVID A. NEWSOME
R&arme--On enregistre I’activite pypillaire dam l’obscuritt a la suite d’une exposition a une huniere intense et on y distingue plusieurs phases: (1) une dilatation initiale, (2) une contraction de quelques millimetres avec des oscillations relativement lentes et de grande amplitude pendant 456 min, (3) une contraction d&croissant graduellement pendant 8-12 min, et (4) une stabilitt a pleine ouverture pupillaire. Dam ces conditions exptrimentales l’apparition de I’ image consecutive positive etait pr&Adee par une latence allant jusqu’il 12 sec. La phase (2) comcide avec l’apparition de l’image consecutive positive et est reduite ou absente chez les sujets avec achromatopsie de bltonnets. La phase (3) se termine avant la disparition de l’image consecutive negative et son evolution temporelle rappelle la recuperation de la sensibilitt des bAtonnets aprea decoloration. Les phenomenes pupillaires et visuals dependent tous deux de l’intensitt et de la d&e du stimulus lumineux d’adaptation. On montre l’analogie entre oscillations pupillaires en presence d’images consecutives et en presence de lumieres extb rieures stables de luminositt semblable. On discute divers m&anismes qui peuvant expliquer ces phCnomenes. Zusrunme&srBHrg-Es wurde die Pupillentatigkeit im Dunkeln nach starker Belichtung registriert und als sich in genauen Phasen abspielend befunden: (1) einer anf&nglichen Ausdehmmg folgt (2) eine Zusammenziehung von einigen Miilimetem mit verhitltnismiissig langsamen 4,5 bis 6 Minuten langen Schwingungen von grosser Amplitude, (3) eine Phase einer langsam abfahenden 8 bis 12 Minuten langen Z usammenziehung ohne Umuhe und (4) eine stabile Pupille, nachdem die volle G&se erreicht worden war. In diesen Versuchsbedingungen ging der Erscheinung eines positiven Nachbildes eine Latenzzeit von bis zu 12 Sekunden voraus. Die Phase der durch Umuhe begleiteten Pupillenwiederzusammenziehung fiel mit der Prscheinung des positiven Nachbildes zusammen und war in Stlbchenmonochromaten geschwiicht oder abwesend. Die spiitere Phase der langsam abfallenden Zu sammenziehung beendete sich, ehe das negative Nachbild verschwinden konnte und folgte einem Zeitlauf, welcher sich der Erholung der Stabchenempfindlichkeit nach Ausbleichung Bhnelte. Sowohl die Pupillen- als such die Schphinomene hingen von der Starke und Dauer des Umstim-
mungslichtes ab. Die dem Nachbild und einem lusseren gleichhelligen Licht gegentirtigen Pupillenschtingungen 8hnelten einander. Es werden einige diesen Pharromenen mbglicherweise. unterliegende Mechanismen erortert. Jbuna~e~b~arr aKMBHocTb 3pauKa B TetuHoTe, nocne ~KC~O~H~HHna chewy PB3BJMe 6OJrbLHOH#HWrClH, 6r.r~ra3a~lWrpapOBana; OKa3aJWCb, ‘IT0 OHa XapaKTepE3yeTCK HeCKOJbI(HMH @a3armf, a memo: (1) ~a~arrbrroe pacnmpeHrre, nocrrezryrornee (2) cyxremre na rrecxonbxo WB, c o~~OcHTeHbu0 hieQneHH5rhHr, BbtCOKO-~JrHhUHi OCIlkuuuRlAIIMH 3pa¶ra, B -reKeHHe4,5-6,0 r+nrriyr; (3) @a3a nornenemroro cnorot8noro pacnnrpemta spaspa B TeKeHHe g-12 MHHyT H (4) nocroaHHaa BenBqHHa spasua, nocne roro KBK OH norr~~ro pacrmrpHTcK. B ~THX 3KcneprrMeHTaBBHbrx yc.~o~~~x normneHHro ~OJIOHHT~HB Itor rrocJleKOBaTenBHOro o6pa3a npeAmecTBoBaB HaTeHTHbrHITepEOA B 12 CeKyHH. Oa3a BTOpH‘IHOn, cyWHHK 3pa¶Ka, BO BpeMB KOTO&Xdk na6monamrcb OcuAJTJnmmt,cortnan(ana c noaruremrehr
nonoxsrrw~~oro rmurenona~ olipasa, HO ona 6r.ma penymrponana mm orcyrcrnoBaJra y IWHWHTOB c naHo¶KoBoft axpoA4aToncEeH. DocneHyroman l#Wa rrocTeneHHoro pacrmrpe~~~ 3panxa (nocrerre~or-0 yMeHbrneRaR ~orrrpa~~ypbr era) 3arrBAIHBBeTCK nepen EC%%HOB~HH~M HeraTHBHoro nocHeHoBaTenbHoro 06pa3a H no epehfeHH coBna,rtaer c XOHOM HoccmHoBneHHa rrano~~oloeoB ~y~c~~~~enbuoc~~ nocne 3acBeTa. &uro HaHneHo, PTO o6a 3pa¶KOBb@ H 3pHTeJ5Hbrit 3aBHCaT OT HHTWKJHBHOCTH H ,WTHTeJtbHOCTH BBJreHHK wtrrero -Ha. Gbmo noKa3aHo cxoxcTBo octmmmtmH 3pa’tKa B mWIyTcTBHE noc.rre~oB8TwrbHBrx o6pa3oB H B lQHtcyTcrBHH nomo9mHoro cBcTa, 6wsKoro no cBeTnoTe 3lHM o6pa3ahr. 06cyKrHaroTca HeKOTOpBJeBo3MOxrHMe MexaAA3hrbt 3THx rfB.neBHH.
Res. Vol. II. pp. 275-288.PorgamonRes
AFTERIMAGE
1971.Printedin Grut
Britain.
AND PUPILLARY ACTIVITY FOLLOWING STRONG LIGHT EXPOSURE DAVID A. NEWSOME
Ophthalmology Branch, National Eye Institute, National Institutes of Health, U.S. Department of Health Education, and Welfare, Bethesda, Maryland 20014, U.S.A. (Received 30 April 1970; in revised form 29 June 1970)
INTRODUCTION PUPILLARY behavior in darkness after exposure to pre-adapting luminances of weak or
moderate intensity has been measured (REEWS,1918; YOUNGand B~nrsw~~, 1954), but activity following extremely bright light has received little attention. ALPERN and CAMPBELL (1963) reported that, after 3 min adaptation to intense light, the pupils in darkness first dilated and then reconstricted. They interpreted their findings as showing that the retina under these conditions continued to activate the pupil in the absence of external stimuli. A re-examination of this phenomenon was undertaken, using a method that allows continuous recording of pupil size in darkness. The results in this report confirm Alpem and Campbell’s findings; in addition, some previously undescribed aspects of pupillary activity after strong light exposure and their intimate association with afterimages are presented. METHODS Nine normal young adults participated. Detailed observations were made on six of these. Pupillary activity was recorded continuously by the electronic infrared pupillograph of LG~ and LOEWENFELD (1958). The subjects sat in a dark room withchii and forehead supported, and their eyes shielded from the stray light of the instrument. After 10-15 min dark adaptation, the subjects occluded the right eye and tixed with the left on the center of a 17 x 20’ quadrangle of about 3-5 x lo6 trolands brightness. The intensity of this light was measured to be about 10 log units above scotopic visual threshold (see Fig. 1). The standard light stimulus consisted of a 2-min exposure to this iield. As soon as the light was turned off, recording of pupil sire was begun. Pupillary movements were recorded continuously for 10-15 min; thereafter, 15-30 set long tracings were made at l-min intervals up to 30 min in darkness. In most sessions no fixation light was used; the subjects maintained steady gaxe with no reported ditliculty. When used, the fixation point was 5 mm/dim red spot, l-m distant, viewed via the front surface mirror of the pupillograph. One-minute and longer exposutes to the bright adapting light were separated by at least 24 hr; with short (30 set or less) or less intense light stimuli, about 1 hr was interposed between exposures. Intensity of the light stimuli was varied with Wratten neutral density filters, and stimulus duration by a hand switch and stop watch.The subjects controlled an event marker on the pupillograph tracing by a hand switch. They were instructed to mark the record (1) when the positive afterimage began to appear, (2) whenever it became brighter, and (3) when it could no longer be seen. The negative afterimage was observed against a field of about O-4log ft-L uniform surface illuminance located 8 ft from the subjects. The ‘end-point” for the negative afterimage came when it could no longer be seen against this background illumination. Condensed tracings of pupil activity were made from the original records by sampling pupil size at 1-set intervals. Since the responses of the stimulated and consensually reacting pupils were equal in all experiments, the trace of only one pupil is shown in the figures. In other experiments pupil activity in a steady dim light was tested. Dark-adaptation time and experimental set-up were unchanged (see Fig. 1) except that the voltage to the stimulator lamp was reduced with a Powerstat so that the field brightness matched approximately the peak intensity of the afterimage. This matching was done by the subjects in preliminary experiments. 275
276
DAVIDA. NIWXIME
EXPERIMENTAL
SET
L!P
#l
PHOTOFLOOD
tNFRARED
SCANNING
8 COLLECTING MULTIPLIER
TUBE
Fro. 1. Bperimental set-up. As the subject sat in darkness, his left eye was e%po& to a 17 x 2tY *Id of about 3-5 x lo6 trolands brightness, after which pupil movements in darkness were
recorded by an electronic i~m-~-~siti~
scanning device.
RESULTS
(1) Pupil actiuify Figure 2 shows the behavior of one subject’s pupils in darkness after a Zmin exposure to the ftil intensity of the adapting Iight. When the light was extinguished, the pupils began to dilate smoothly and rapidly. This dilation had a brief latent period that could not be measured precisely for technical reasons, but was shorter than 0.5 sec. The dilation was I INITIAL
M H
A-Light Off
2 min O Light
I
I
I
I
100
200
300
400
I
500 G&%GG
TIMEIN DARK.see
Fro. 2. Pupil activity in darkness (Subject MH). After a 2-n& exposure to the stimulus light (“light off’ at arrow), the pupils first dilated rapidly, then reconstricted and showed unrest for about 5.5 min. Thereafter the constriction diminished gradualiy and quietly until fully darkadapted sire was reached. The pupils then remained quiet to the end of the experiment. The positive afterimage was first seen after 6 set darkness; the first small arrow shows when it reached maximum brightness, the second when it disappeared, and the thiid when the negative afterimage could no longer be seen.
2n
Afterimage and Pupillary Activity following Strong Light Exposure
but, before the pupils reached dark-adapted sire, they recontracted. This recontraction was not smooth. Rather, it took the form of low-frequency pupillary unrest with swings of large amplitude. The reconstriction with unrest gradually lessened, then disappeared rapidly after 45-6 min, depending on the subject. A phase of gradually diminishing constriction without unrest followed, and, about 15-18 min after “light ofI”, full pupil size was reached. Similar behavior was found in all subjects’ pupils, but details of amplitude and frequency of the oscillations varied among individuals (see Fig. 3). Only one of the nine subjects (DL, see Fig. 4) had an average amplitude of recontraction less than 2 mm (as measured from dark-adapted pupil sire); her pupils recontracted slightly more than 1 mm. For this group of subjects, pupil size at the end of the light exposure was usually about 3 mm, with initial dilation to 6-8 mm. The average diameters at maximum reconstriction ranged between 45-6 mm, and at full dark adaptation between 7-8-5 mm. extensive,
(2) Visualphenomena When the 2-min bright light stimulus was turned off, none of the subjects saw an afterimage immediately. After several seconds of complete darkness a positive afterimage TT Positive
After-image
2
2
I
MT
5 -l4a 3z
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MH
3
I
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I
20
25
30
4
* K I 0
!
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5
IO
15
20
t 25
TIME IN DARK,
0
5
IO
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min
Fro. 3. Four subjects’ pupil activity in darkness after 2 min full-intensity light. These curves show inter-personal variations in (1) average amplitude of recontraction, (2) duration and amplitude of unrest, and (3) the correspondence between duration of recontraction with unrest and duration of the positive afterimage (shown by the bar above each curve).
278
DAVID A. N~wsom
appeared. It grew brighter, peaked, and passed through a series of dimmings and brighten-
ings before gradually fading away. The appearance of the positive af&image cointided with the ~n~~ of the ‘pupillary ~~~~on in darkness- Fading of the a&image was accompanied by the gradual decrease in the amplitude of the pupillary unrest, aud its full disappearance with the beginning of the quiet phase of diminishing constriction toward fully dark-adapted size (see Fig. 2). All subjects were asked to indicate with the event marker whenever the afterimage brightened. This subjective sensation of brightening usually Cain&led almost perfectly with the more marked ~on~~tio~~ of the pupillazy unrest (see Fig. 4)*
L
I
120 t40 TfME fN OARK AFTER
I
I60 STIMULUS
#
L
f&z3 200 EXPOSURE, set
When the positive afterimage had disappeared permanently, the presence of the negative afterimage was followed until it could no longer be seen against the dim iudu~~~~ field. After a full-int~~~ty Z-min light exposure, six subjects could see a negative afterimage for an average of 24-1tin after “fight 0iP (from 224&S min). 1n each case the negative afterimage persisted several minutes after full pupil size in darkness had been reached. (3) Stimulus intensity
The presence and degree of recontraction of the pupils after initial diiation at ““fightoff” depended on the intensi~ and duration of the preceding light stimulus. When stimulus duration was held constant at 2 min while the stimulus in~nsi~ was decreased, duration and amplitude of the following pupillary recontraction with unrest decreased progressively (see Fig. SB, C). When the light intensity had been reduced 2 log units (Fig. 5D), the pupils dilated steadily and rather rapidly to full size without showing recontraction or unrest, even though
Ma-image
I
and Fupii
TT DlJfL7tiOl7 Positive After
Activity followins Strong Lit&t Expomre
A
-image
~
J
Li3 2
I IO
1
1 20
I
L 30
TiME IN DARK.
minutes
Fm. 5. Effkct of clcm&ng intu&ty of light stimuh~~. 7% same subject was given four 2-e tight stimuli, with the brightncnsprogmssively diminished fmm fti intensity (A). The period of pupikry recontraction with unrest was progressively diminished when the lit was reduced by O-6 log units (II), and l-6 log units Q; it was absent when a 2-Olog filta: was
interposed (D). With the weakest light them was no latent period for the positive afterimage.
the afterimage did (subjectively) fluctuate in brightness. With this reduced stimulus intensity there was no latent period for the positive ~te~rna~. (4) Stimulus duration Papillary activity and afterimage phenomena varied also when the intensity of the preceding light stimulw was held constant and its duration changed. With fidl stimulus intensity and exposure times shortened progressively, the period of recons~ction with unrest became shorter, and disappeared entirely with stimuli shorter than 1 set (see Fig. 6). When the subjects were shown the bright light stimulus for only 0.5 set, all saw the afterimage immediately at “light off”. The minimum light exposure required to produce a latent period before the appearance of the positive afterimage varied from subject to subject, ranging between 1 and 5 sec. The duration of the latent period increased with the duration of the preceding light, reaching a plateau after 2 min exposures (Fig. 7). (5) Pupillary activity after brief light stimuli With bright light stimuli of 1 set or less the pupil behaved differently than with longer
MH
a
A
J
t0sec Light
I
1
I
1
1
I 2 3 4 5
1
IO
I
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I
20
I
30 D
Light
Light TIME IN DARK,
min
FIG. 6. Effect of decreasing duration of the light stimulus. The same subject was given the full intensity light stimulus for exposures up to 4 min (D). Decreasing the duration of exposure to 1 min (c) and then to 10 set (B) shortened the length of the afterimage latent period, lowered the peak of the initial pupil dilation, and diminishedthe extent and duration of the rccontraction with unrest. When the Hposure was for only 1 set (A), the afterimage was seen immediately, and pupillary recontraction was absent.
stimuli: at the end of the light exposure it remained contracted for a few seconds before dilating with little or no unrest and no recontraction phase (see Fig. 8). In addition, the afterimage latent period was missing after’such short, high intensity light stimuli. (6) Retinal hypoxia Two subjects produced what was presumed to be transient hypoxia of the retina by exerting finger pressure on the Fre-exposed left globe. When this was done, the pupils dilated. When pressure was released and the afterimage reappeared simultaneously the pupils again contracted (see Fig. 9). Pressure on the non-stimulated right eye did not afkt pupil size. (7) Pupillary oscillations in dim steady light In two subjects the left eye was exposed to the same stimulus field as already described, except that the light intensity was dimmed to a level matched as closely as possible to the
Afterimage and Pupillary Activity following Strong Light Exposure
0
5
IO
30
I
2
see
281
4
3 min
DURATION
OF STIMULUS
LIGHT
Fro. 7. Infiuence of duration of light stimulus on latent period of afterimage. (Pour different subjects, full light intensity.) With ail other parameters constant, the stimulus duration was lengthened from 0.5 set to 4 min. Stimulus time above 2 min produced little further increase in latency of the positive afterimage.
RB
8r -
Lighl
k?
2
I I
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2
3
4
5 TIME.
I
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I
,
I
6 see
7
8
9
IO
FIG. 8. Prolonged pupil contraction after brief flash of intense light (subject RB). After a 05 set flash of light about 10 logs above scotopic visual threshold (. . . . . .) the pupillary contraction lasted much longer than that elicited by an equally long but less intense light flash about 75 logs above threshold). In both cases the positive afterimage was seen (-, immediately.
peak intensity of the afterimage (see Methods). In the presence of this steady, dim light the pupils showed unrest resembling closely that observed in the afterimage experiments. The similarity of the same individual’s unrest under these two different conditions, and variations between subjects, are illustrated by the frequency analysis for pupil oscillations of different amplitudes shown in Fig. 10.
282
DAMD A. Nawso~e
t3egin Pressure OS
OFF
00
Begin Pressure
OFF
00
2L
t 80 TIME,
I
t
90
iOU
set
FIG. 9, Effect of retinal hypoxia on Pupillary recontraction after exposure to bright light. During the period of recontraction in darkness (75-100 set after 2-min bright light stimulus) the subject pressed firmly on the stimulated eye (OS, 0 C?0 01, or on the unstimutated eye (OD, * *a e,2. when the retina of the stirdated eyewasmade iscbemic in this way the aftarimage disappeared and the pup% dilated; they reconstricted when pressure was r&a& (arrow, “‘OFF”]. When the unstimulatedeye wascompressed,the pupils remained contracted.
DISCIJSSION Under the conditions used in these experiments, pupillary activity following very bright light stimtii showed three distinct phases: (1) an initial pupillary dilation, lasting several seconds, (2) marked pupillary reconstri~io~ with unrest, beginning with the appearance of the positive afterimage and lasting between 4.5 and 6 min, and (3) a final phase of quietly diminishing contraction lasting 8-12 min and ending when full dark-adapted pupil diameter was reached, before the disappearance of the negative afterimage. In this sequence of events three main phenomena appear to play a role. These will be discussed separately.
The pupiIlary reconstriction observed in these experiments was extensive and long-lasting, What is the source of this activity? It could be thought that the constriction was produced as the subjects accommodated on the positive afterimage when it appeared. However, the pupils reacted the same when the subjects looked at a far fixation spot during the test and when they did not. Furthermore, pupiftary re~ntra~ion occurred only after iight stimuli 940 log units above scotopic visual threshold. A diminution of stimulus intensity by 2 logs abolished the recontraction phase and the pupils dilated smoothly and quickly, even though a positive afterimage was seen.
283
Afterimage and Pupillary Activity following Strong Light Exposure
MATCHED,
STEADY
DARKNESS
LIGHT
WITH
AFTERIMAGE
GH
i
i
8 9 EXTENT
*I
OF CONTRACTIONS.
I23456769 tenths
of mm
FIG. 10. Frcqmmcy pattern of pupiihuy oscillations under two different experimental conditions (two subjazts). In each experiment the amplitude of all individual pupil oscillations The ordinate shows the number of pupil o6mmingwithina130aactimapcriodwasoscillations and the abscitm amplitude of them ~WJ (ii O-l-mm units). The intensity of the steady dim light was matched ~p1clo~ly~m_~lc to the peak brightness of the positive .
Fatigue can produce extensive pupillary oscillations (LOWJSNSTEIN, FEINBERG and LOE1963), but in normal subjects these are not seen so soon after the beginning of the experiment, and since the pupils eventually became large and quiet after dark adaptation, the subjects were undoubtedly alert. The timing of the initial phase of marked pupillary contraction (456 min) and of the following phase of gradually diminishing contraction (8-12 min) suggests that the first contraction phase may be related to cone function, and the following phase to rod function. The coincidence of the positive afterimage with the first recontraction phase, and of the subjective negative afterimage with the phase of diminishing contraction supports this view. To test the dependence of the pupillary constriction on cone function, two persons with rod achromatopsia were examined using the full stimulus intensity for 2 min (see Fig. 11). The period of recontraction with unrest was absent entirely in one of them (GE) and markedly attenuated in the other (DM). This latter observation is consistent with the fact that DM had a few functioning cones (G~URQ and GUNKEL,1964). With shortening exposure to the stimulus light, DM’s pupils-just as those of the normal subjects-took less time to reach full diameter. Both the subjects with rod achromatopsia saw amorphous, short-lived afterimages compared to the sharply etched images described by the normal subjects. DM’s drawing of what she saw, along with what a normal individual drew, is shown in Fig. 12. Cone function appears, then, necessary to the phenomenon of marked pupillary recontraction after exposure to very bright light. The rods-probably responsible for the second WDIFELD,
DAVIDA. N-
284
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FULL LIGHT
:
.
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---
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32I
5
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I
f
IO 20 I5 TIME IN DARK. min
I
I
25
30
Flo. 11, Pupil&y movements after bright light exposure in persons with rod achromatopsia (two subjects). The upper curve shows the movemcuts of GE’s pupils after a 2-min exposure to the bright adapting light. Note the absence of reconstriction with unrest, and the comparatively brief duration of the positive afterimage. The tower three curves show the nsponsas of DM’s pupils after progressively longer full-intensity light stimuli. After the 2-min exposure to full stimulus intensity (. . . . . .) there was a small amount of re~onstriction.The differenceain final pupiIs sizes for this subject is explained by the fact that the experiments were run on separate days.
phase of dim~shing contraction-ap~r to be mu& less effective in activating the pupil under these conditions than are the cones. This assumption fits well with the characteristics of pupiflary reactions elicited via the rods in other experiments: while the pupi~omotor threshold of the retinal periphery is much lower than that of the fovea (particularly when blue light is used), its motor efficiency is quite low (see, LOWENFELD,1966, Summary).
The latent period for the appearance of the positive afterimage, accompanied by fast pupilllary dilation during the first seconds in darkness, reflects an absence of afferent (visual and pupillary) stimulation immediately after prolonged exposure of the retina to powerful light. Such an absence of retinal discharges could be due to photochemical mechanisms (compare BRINDLEY,1962) or to neural influences, that is, temporary cessation of conduction by retinal neurones, In other words, the threshold for pupillary (and subjective visual) responsiveness may have been raised so high by the intense retinal stimulation (or bleaching)
Afterimage and Pupillary Activity following Strong Light Exposure
285
FIQ. 12. Afterimage of normal subject and of one with rod achromatopsia. After a 2411 exposure to the 17 x 20” field at brightness, normal subjects reported seeing a sharply outlined, lemon colored afterimage with a contrasting magenta halo, as shown on the left. Under the same conditions a subject with rod achromatopsia saw the “fuzzy” afterimage which was drawn as shown on the right. The subject saw no color.
that the system fails to respond to the relatively low intensity of the afterimage activity until some retinal dark adaptation has taken place. That such an inability to respond to weak stimuli really exists is shown by the following experiment. One of the subject’s eyes was exposed for 2 min to the full-intensity stimulating light. When the afterimage appeared after “light off”, the subject matched as closely as possible the intensity of the stimulus field (reduced by rheostat) to the peak brightness of the positive afterimage. In subsequent experiments the eye was again stimulated for 2 min at full intensity. Beginning 1 set after “light off”, the previously matched light was presented during the period of initial rapid pupillary dilation. This stimulus was not seen, and did not affect the pupil until about 0.5 set after the positive afterimage appeared. The afterimage latent period and the coincident rapid pupillary dilation depended on the total energy of the adapting light. As full stimulus intensity was reduced, or as the light was shortened, the latent period for the afterimage and the peak of the initial dilation were reduced. In fact, with very short full intensity stimuli the pupillary constriction outlasted the stimulus up to several seconds, and the full brightness of the afterimage was seen immediately at “light off”. In view of the relatively short duration of the afterimage latent period with pupillary dilation it appears likely that these phenomena are caused by cessation of neural conduction rather than by a sudden interruption of the relatively long lasting photochemical process. The afterimage also disappeared and the pupil dilated when blood flow to the eye was impeded by pressure. This similar phenomenon is known to be caused by loss of conductivity of the neural elements due to hypoxia of the retina. A number of authors have described retinal damage in animals by visible and invisible light energy (NOELL, WALKER, KANG and BERMAN,1966; KUWABARA and GORN, 1968) and recently DAWSON and HERRON (1970) showed that in normal human subjects prolonged exposure to the full intensity of an indirect ophthalmoscope raised dark adaptation thresholds during the first 8 min after exposure. Dawson and Herron pointed out that a large amount of infra-red radiation is produced by tungsten sources such as the ophthalmoscope lamp. Since our light source was also tungsten, it seemed of interest whether an intense adapting light with very little infra-red energy would also produce the afterimage latency phenomena. A Grass
Dc;vn, A. Ntwsom
286
photic stimulator was used, via an infra-red reflection titer (100 &she&z, flash duration S-msec, intensity 9.3 log units above scotopic visual threshold). Following 2 min adapting exposures to this light, more than 3 set elapsed before the afterimage could be seen. (3) Oscillatory behavior During the first, marked recontraction period both the pupils and the afterimages showed fluctuations that usually coincided. It therefore appears reasonable to assume that the retina is the source of these fluctuations. Each subject had a distinct pattern of oscillations repeatable in successive tests; and for each person a similar pattern of pupillary unrest was recorded in the presence of steady, dim light of an intensity matched approximately to the brightness of the afterimage. Under these conditions the subjective visual sensation did not fluctuate, and yet the pupil did. While we cannot explain why there is similar pupillary activity in the absence of subjective (visual) fluctuations, such pupillary oscillations in the presence of steady illumination are well known, and have played a considerable role in the clinical literature under the names of “pupillary unrest”, or, if marked, “hippus” (see 1969, Summary). The rate and amplitude of such lightL~WENST~N and LOW, induced pupil unrest depend primarily upon the intensity of the illumination and secondarily upon personal characteristics, that is, unrest tends to be most ample in young, excitable individuals. The particular pattern of oscillations for each individual is determined by genetic factors as shown by the fact that the pattern is the same in identical twins (see Fig. 13).
LIGHT
INTENSITY,
log,o
units
Fro. 13. Patternof pupil oscillations in five normal subjects under influence of lights of varying intensity.1 The ordinate represents the average amplitude of each subject’s pupil oscillations occurring within a 2OO-secperiod for each light intensity step marked on the abscissa. (23 Year old men; (. . . . . .), 25 year old man; (- - - -), 21 year old woman. u. W), dak from identical (monozygotic) 23 year old male twins. Note that the amplitude protile diikr considerably among the unrelated subjects. These profiles were found consistently for each individual in repeated tests. Between the identical twins the values were as similar as were two successive exp&ments in the same individual. 1 Unpublished experiments (I. E. bJEWENFELD ) from the Lowenstein Laboratory of Pupillmphy, Columbia University, College of Physicians and Surgeons, Department of Ophthalmology.
Afterimageand Pupillary Activity followingStrong Light Exposure
287
This light-induced pupillary Unrest is assumed to be elicited by afkrent stimuli at a central nervous site, probably the oculomotor nucleus (YOUNGand BIERSDORF,1954). The precise mechanism is unknown. Acknowlcdgcmcnts-The author is grateful to Dr. IRENE~F3vENm.D and Dr. Parart Gosuggestions in this study.
for their helpful
SUMMARY Pupillary activity in darkness following exposure to strong bright light was recorded and found to occur in distinct phases, namely, (1) an initial dilation followed by f2) reumtraction of several m&meters with relatively siow, l~~~~tu~ pupillary osciltations for 4.5-6 min, (3) a phase of gradually decreasing contraction without unrest Ming 8-12 min, and (4) stable pupils after full sire was regained. Under these experimental conditions the appearance of a positive afterimage was preceded by a latent period up to 12 sec. The phase of pupillary recontraction with unrest coincided with the appearance of the positive afterimage, and was reduced or absent in patients with rod achromatopsia. The later phase of gradually diminishing contraction ended before disappearance of the negative afterimage and had a time course rdmilar to that for recovery of rod sensitivity after bleaching. Both pupil& and visual phenomena were found to depend on the intensity and duration of the adapting stimulus fight. Similarity of pupilhuy oscillations in the presence of the af&mage and in the presence of an external steady light of similar brightness was shown. The oscihations have not been noted previously. REFERENCES ALPERN, M. and CAMPBELL,F. W. (1963). The behavior of the pupil during dark adaptation. J. Physfof. 165 5-7. I3rmmrx~,G. S. (1962). Two new propertiesof foveaI after-imagesand a photochemical hypothesis to explain them. J. Physiol. 164,168-179. DAWSON, W. W. and Hrmto~, W. L. (1970). Retina1 i&mination during indirect ophthalmoscopy: Subsequent dark adaptation. Zest. Ophthd 9,89-96. GOURAS, P. and GUNKEL,R. D. (1964). The frequency response of normal, rod achromat and nyctalope ERGS to sinusoidal monochromatic light stimulation. Documenfa Opthul. 18,137-1x). KUWABARA, T. and GORN,R. A. (1968). Retinal damage by visible light: An electron microscope study. Arch. Ophthal. 79,69-78. Lo~wzmw,
I. E. (1966). Pupiky rno~~ associated with light and near vision: An exp&menta! review of the literature. In Recent Deocfupments in Vision Research (edited by M. Wmrcam), National Academy of Sciences, National Research Council, Washington, pp. 17-105. ~WENSRSN, 0. and bEwENIm& I. E. (1958). Electronic pupillography. A new imtrumant and some clinical applications. Arch. Ophthul. 59,352-363. ~wEN~~~J, 0. and bEWENF&D, I. E. (1%9). The pupil. In The Eye (edited by H. D~vso~), 2nd Edn., Vol. 2, Academic Press, New York, pp. 276-277. L~WENSJZIH, 0.. FEINISERG, R. S. and L~~EXFEL,D, I. E. (1963). Pupillary movenents during acute and chronic fatigue. Znvest. ~~~t~i. 2,138157. Now, W. K., WALKER,V. S., KANG,B. S. and BF.RMAN, S. (1966). Retinal damage by hght in rats. 1-t.
Ophthal. $450-473. REEVFB,P. (1918). Rate of pupillaty dilation and contraction. Psychol. Reo. X$330-340.
YOUNO,F. A. and BIERSWRF,W. (1954). Pupillary contraction and dilation in light and darkness. J. camp. physiol. Psychol. 47,264-268.
~~-~pi~i~ activity in darkness following exposure to strong bright light was reoorded and found to occur in distinct phases, namely, (1) an initial dilation followed by (2) recontraction of several milliietem with relatively slow, large-amplitude pupillary oscillations for 4.56 min, (3) a phase of gradually decreasing contraction without unrest lasting 8-12 min, and (4) stable pupils after full sire was regained. Under these experimental conditions the appearance of a positive afterimage was preceded by a latent period up to 12 sec. The phase of pupillary recontraction with unrest coincided with the appearance of the positive afterimage, and was reduced or absent in patients with rod achromatopsia. The later phase of gradually finishing contraction ended before disappearance of the negative afterimage and had a time course similar to that for recovery of rod sensitivity after bleaching. Both pupillary and visual phenomena were found to depend on the intensity and duration of the adapting stimuius light. Similarity of pupillary oscillations in the presence of the afterimage and in the presence of an external steady light of similar brightness was shown. Some possible mechanisms for these phenomena are discussed.
DAVID A. NEWSOME
R&arme--On enregistre I’activite pypillaire dam l’obscuritt a la suite d’une exposition a une huniere intense et on y distingue plusieurs phases: (1) une dilatation initiale, (2) une contraction de quelques millimetres avec des oscillations relativement lentes et de grande amplitude pendant 456 min, (3) une contraction d&croissant graduellement pendant 8-12 min, et (4) une stabilitt a pleine ouverture pupillaire. Dam ces conditions exptrimentales l’apparition de I’ image consecutive positive etait pr&Adee par une latence allant jusqu’il 12 sec. La phase (2) comcide avec l’apparition de l’image consecutive positive et est reduite ou absente chez les sujets avec achromatopsie de bltonnets. La phase (3) se termine avant la disparition de l’image consecutive negative et son evolution temporelle rappelle la recuperation de la sensibilitt des bAtonnets aprea decoloration. Les phenomenes pupillaires et visuals dependent tous deux de l’intensitt et de la d&e du stimulus lumineux d’adaptation. On montre l’analogie entre oscillations pupillaires en presence d’images consecutives et en presence de lumieres extb rieures stables de luminositt semblable. On discute divers m&anismes qui peuvant expliquer ces phCnomenes. Zusrunme&srBHrg-Es wurde die Pupillentatigkeit im Dunkeln nach starker Belichtung registriert und als sich in genauen Phasen abspielend befunden: (1) einer anf&nglichen Ausdehmmg folgt (2) eine Zusammenziehung von einigen Miilimetem mit verhitltnismiissig langsamen 4,5 bis 6 Minuten langen Schwingungen von grosser Amplitude, (3) eine Phase einer langsam abfahenden 8 bis 12 Minuten langen Z usammenziehung ohne Umuhe und (4) eine stabile Pupille, nachdem die volle G&se erreicht worden war. In diesen Versuchsbedingungen ging der Erscheinung eines positiven Nachbildes eine Latenzzeit von bis zu 12 Sekunden voraus. Die Phase der durch Umuhe begleiteten Pupillenwiederzusammenziehung fiel mit der Prscheinung des positiven Nachbildes zusammen und war in Stlbchenmonochromaten geschwiicht oder abwesend. Die spiitere Phase der langsam abfallenden Zu sammenziehung beendete sich, ehe das negative Nachbild verschwinden konnte und folgte einem Zeitlauf, welcher sich der Erholung der Stabchenempfindlichkeit nach Ausbleichung Bhnelte. Sowohl die Pupillen- als such die Schphinomene hingen von der Starke und Dauer des Umstim-
mungslichtes ab. Die dem Nachbild und einem lusseren gleichhelligen Licht gegentirtigen Pupillenschtingungen 8hnelten einander. Es werden einige diesen Pharromenen mbglicherweise. unterliegende Mechanismen erortert. Jbuna~e~b~arr aKMBHocTb 3pauKa B TetuHoTe, nocne ~KC~O~H~HHna chewy PB3BJMe 6OJrbLHOH#HWrClH, 6r.r~ra3a~lWrpapOBana; OKa3aJWCb, ‘IT0 OHa XapaKTepE3yeTCK HeCKOJbI(HMH @a3armf, a memo: (1) ~a~arrbrroe pacnmpeHrre, nocrrezryrornee (2) cyxremre na rrecxonbxo WB, c o~~OcHTeHbu0 hieQneHH5rhHr, BbtCOKO-~JrHhUHi OCIlkuuuRlAIIMH 3pa¶ra, B -reKeHHe4,5-6,0 r+nrriyr; (3) @a3a nornenemroro cnorot8noro pacnnrpemta spaspa B TeKeHHe g-12 MHHyT H (4) nocroaHHaa BenBqHHa spasua, nocne roro KBK OH norr~~ro pacrmrpHTcK. B ~THX 3KcneprrMeHTaBBHbrx yc.~o~~~x normneHHro ~OJIOHHT~HB Itor rrocJleKOBaTenBHOro o6pa3a npeAmecTBoBaB HaTeHTHbrHITepEOA B 12 CeKyHH. Oa3a BTOpH‘IHOn, cyWHHK 3pa¶Ka, BO BpeMB KOTO&Xdk na6monamrcb OcuAJTJnmmt,cortnan(ana c noaruremrehr
nonoxsrrw~~oro rmurenona~ olipasa, HO ona 6r.ma penymrponana mm orcyrcrnoBaJra y IWHWHTOB c naHo¶KoBoft axpoA4aToncEeH. DocneHyroman l#Wa rrocTeneHHoro pacrmrpe~~~ 3panxa (nocrerre~or-0 yMeHbrneRaR ~orrrpa~~ypbr era) 3arrBAIHBBeTCK nepen EC%%HOB~HH~M HeraTHBHoro nocHeHoBaTenbHoro 06pa3a H no epehfeHH coBna,rtaer c XOHOM HoccmHoBneHHa rrano~~oloeoB ~y~c~~~~enbuoc~~ nocne 3acBeTa. &uro HaHneHo, PTO o6a 3pa¶KOBb@ H 3pHTeJ5Hbrit 3aBHCaT OT HHTWKJHBHOCTH H ,WTHTeJtbHOCTH BBJreHHK wtrrero -Ha. Gbmo noKa3aHo cxoxcTBo octmmmtmH 3pa’tKa B mWIyTcTBHE noc.rre~oB8TwrbHBrx o6pa3oB H B lQHtcyTcrBHH nomo9mHoro cBcTa, 6wsKoro no cBeTnoTe 3lHM o6pa3ahr. 06cyKrHaroTca HeKOTOpBJeBo3MOxrHMe MexaAA3hrbt 3THx rfB.neBHH.