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Effect of reduced retinal illuminance on the pupillary near reflex
C:wn
Rtir.
Vol. 9. pp. 1159-I266
Pcrgamoo
Press
1969.
Pnnted in Great Britain.
EFFECT OF REDUCED RETINAL ILLUMINANCE ON THE PUPILLARY NEAR REFLEX1 NILES ROTH Jules Stein Eye Institute, Department of Ophthalmology, UCLA School of Medicine, Los Angeles, California 90024 (Received 5
March
1969)
INTRODUCTION PUPILLARY constriction that occurs when a normal observer changes fixation from far to near has been studied by a number of investigators with a view to determining possible relations to accommodation and the various components of convergence (FRY, 1945; MARC and MORGAN, 1949, 1950; KNOLL, 1949). MARG and MORGAN (1950) concluded that, under normal conditions, the pupillary near reflex is elicited principally by accommodation with fusional convergence playing a minor role in some subjects and none at all in others. Moreover, pupillary diameter as a function of accommodation was found to be linear, although in some cases, only after about the hrst diopter of accommodative response. In general, the findings of Marg and Morgan agree with those of Knoll. An additional aspect of near reflex pupillary constriction and accommodation that will be considered here is the effect of reduction of retinal illuminance on the quantitative relationship between these two functions. As the retina adapts to lower illuminance levels, pupil size increases, provided the accommodative levels remain constant (LE GRAND, 1957). Thus, at photopic levels in the accommodating eye, pupil constriction associated with increased neural stimulation of the ciliary muscle and pupil dilation accompanying reduced retinal illuminance antagonize each other. Although it is recognized that the adverse influence of spherical aberration on retinal image becomes more serious as the pupil dilates, the traditional view is that maintenance of image clarity becomes secondary to attainment of maximum sensitivity as illumination levels drop below photopia. Thus, a larger pupil is more advantageous at reduced illuminances because more of the available light is collected. If the above view is correct, the ratio of change in pupil size to change in accommodation would be expected to diminish at lower illuminance levels, so there would be as little interference as possible with the collecting of quanta by the eye. The purpose of this study was to determine whether the relationship between pupil constriction and accommodation does indeed vary significantly as a function of retinal illuminance when. the latter is altered over a range that includes the transition zone between photopia and mesopia. MATERIALS
AND METHODS
Simultaneous records of accommodative response and pupil means of an automatic optometer with pupillograph attachment. records of refractive change that are not influenced by variations greater than 4.5 mm. Conversely, the pupillographic information,
size change, in the same eye, were obtained by This device is capable of providing continuous in pupil size, provided pupa diameter remains consisting of oscillograph records and infrared
t This investigation was supported by a PHS Research Grant NB-2709 from the National Institute of Neurological Diseases and Blindness, Bethesda, Maryland. 1259
NiLEs RorH
I160
pupil photographs, is not affected by changes in ocular refractive power (ROTH. 1965). Under normal viewing conditions, retinal illuminance is influenced by fluctuations in pupil size. Thus. as mentioned eariier, when the pupil constricts with a change in fixation from far to near. pupiltary light response opposes near reflex constriction with compensatory dilation. Therefore, if the aim is to study the pupillary near reflex as separate from the light retfex, the accommodative stimulus must be controlled in the laboratory, SO that retinal iliuminance is independent of pupil size. MARG and iMORCAZi (1949) avoided interaction between the light and near reflexes of the pupil by adjusting the target luminance at each fixation distance for a standard flicker rate. Thus, they maintained, a constant retinal illuminance for all fixation distances and pupil size variations occurring with changes in fixation distance could be ascribed to factors separate from the pupillary light response. The present investigation utilized a different means of avoiding interaction between light and near reflexss of the pupil. This consisted of an optical system in which the target was seen through an exit pupil, 3 mm in dia., centered around the visual axis and located in the plane of the entrance pupil of the test eye (ROTH, 1966). The minimum natural pupil diameter for ail subjects was always considerably greater than the diameter of the exit pupil of the accommodative stimulus system. so that retinal illuminance remained constant over the range of pupil diameters encountered in this experiment. Target luminance was controlled with neutral filters (ROTH. 1966). Luminance levels ranged from 5.6 x l@t to 5.2 x 10-J miliilamberts (mL).Z When these tuminances are compared with the ievel corresponding to the transition from photopia to mesopia (3 x IO-2 mL, Tschermak), it is seen that five test luminances fall above the upper limit for twilight vision and three below this limit (Table 1). TABLE1, &TlYAL A CONSTANT
ILLUMINANCE
VS. TARGET
LUMINANCE
EFFECTIVE PUPIL DIAMETER OF
3 mm
FOR
(AREA=
7.07 mmz) Target luminance (mL) 0.56
0.28 0.13 0.06 I 0.045 0.023 0.0097 O,OOE
Retinal illuminance Log trolands Trolands (to nearest tenth) 12.6 6.3 2.9 1.4 1.0 0.52 0.22 0.12
1.1 0.8 0.5 0.2 0 -0.3 -0.7 -0.9
Troland values were calculated as follows: Trolands = (mL) (3.18)*(7.07 mmr). * Conversion factor, mL to cd/m’-. Limitations in the apparatus made it impractica1 to correct the subject’s refractive error during the course of the experiment, but near and far target locations coutd be chosen to elicit adequate accommodation for studying near response of the pupil. Excessive accommodation had to be avoided. as it would have been accompanied by pupil diameters smaller than the 4.5 mm minimum demanded by the present methods of measurement. The eleven research subjects of this experiment were male students at the University of California, Los Angeles, ranging in age from 18 to 28 yr. All had prior training with the same apparatus in this laboratory during an earlier experiment (ROTH, 1966): in the present experiment, the subjects participated in a total of 60 trials with two or three day intervafs between trials for a given subject. The accommodative stimulus targets (2-degree field) have been described elsewhere (ROTH, 1965). The experimental procedure
Target luminance was set at 0.56 mL (highest level), and the subject’s eye was aligned in the apparatus. The left eye was occluded and two targets were chosen for the right eye so that approximately one diopter of accommodative response would be elicited on changing fixation from the far target to the near one. Adaptation to the existing illuminance level was determined by observing the pupillographic record as the subject fixated the far target. As soon as a relatively constant pupil diameter was indicated by minimum fluctuation of the pupillographic tracing. the subject was instructed to signal with a buzzer that the target was * Values derived from measurements photometer.
made with a UB-l-I/2
Photoresearch
Corporation
photoelectric
Effect of Reduced Retina! Illuminance on the Pupillary Near Reflex
1261
seen clearly. Following this signal, a pupil photograph was taken, the far target was replaced with the near one, the subject signaled again when he saw the target clearly, a second photograph was taken, the far target was restored. and the test sequence ended with a final signal from the subject that the far target was seen clearly. The foregoing six occurrences, spanning an interval of about 10 set, were recorded by the event marker of a pen recorder that also recorded in separate channels simultaneous accommodative and pupillary responses on the same time base. Infrared photographs were measured later and pupil size data inserted into the record at positions on the time scale indicated by the appropriate event marks (Fig. 1).
2
L
FIG. 1. Simultaneous records of accommodative response (I) and relative pupil area (2). Marks in event trace (E) indicate: B,-subject’s signal that far target is clear; P,-camera shutter open for first pupil photograph; N-near target in view; Ba-signal that near target is seen clearly; P?-camera shutter open for second pupil photograph; BsYsigna! that far target is seen clearly. Remaining equally spaced marks in trace E indicate I-set intervals. Figures above pupillograph trace (2) show pupil diameters (mm) obtained later by measuring pupil photographs. The above described procedure was carried out for eight different target luminances in descending order of magnitude. Four additional (retest) sequences were conducted by repeating, in ascending order of magnitude, tests with the four levels above the lowest one. Thus, a total of 12 test sequences were run in each trial, using eight luminance levels. The additional four tests were intended to reveal any fatigue effects that might have influenced the relationship between accommodation and near reflex pupillary constriction at the lowest retina! illuminances. In the preliminary design of the experiment, presentation of target luminances in random order of magnitude was considered and later rejected; experience showed that if the trial duration exceeded a half hour, unstable records resulted from most subjects. Random presentation would have required that the subject adapt to occasional markedly different retina! illuminance levels from ‘one sequence to the next. The additional time needed by the subject to adapt to these large illuminance changes might have introduced the risk of instability in the records. RESULTS
At each retinal illuminance level, relationships between near reflex pupil constriction and accommodation are shown by the ratio of average change in pupil diameter (mm) to average simultaneous change in accommodative level (diopt). For convenience, this quotient is designated “PA ratio” (KNOLL, 1949). Data from 9 of the 11 subjects appeared similar enough to suggest composite treatment of the results (Table 2). Part of the variability in PA ratio at each retinal illuminance level is probably due to influences that are separate from either retinal illuminance or accommodation (LOWENSTEIN and LOEWENFELD, 1962). The two remaining subjects will be considered separately. The data of Table 2 (9 subjects) were analyzed with respect to significance and linearity of the relationship between PA ratio and retinal illuminance. The estimated mean slope of the regression curve of PA ratio on log trolands is -0.14; i.e. the change in pupil diameter associated with one diopter of accommodation diminishes at an average rate of about 0.14 mm per log unit as retinal illuminance decreases. This reduction in PA ratio is statistically significant at the 0.5 per cent level and a test of the linearity of regression by
NILES ROTH
1261
TABLE 2. PA RATIOS AT 8 RETINAL ILLIMINANCE LEVELS FOR 9 SUBJECTS. RETEST \.ALUESARE SHOWN PARENTHESES
I.1
0.8
0.j
0.2
Log trolands 0
T.B. A.De. A.F. A.D.G C.G. P.J.H. L.L. G.M. J.W.
-0.16 -0.32 -O.jl -0.M -0.j3 -0.10 -0.29 -0.16 -0.u
PO.37 -0.07 -0.09 -0.29 -0.69 -O.-l1 -0.x -0.12 -0.25
-0.37 -0.03 --0.45 -0.34 -0.12 --0.10 --0.16 -0.11 -0.2j
-0~35(-0~25) -0.02( -0.08) -O.lj(-0.19) -O.l7(-0.38) -0.2-I-O.lj) -0.20(-0.10) -O-14(-0.17) -o~lo(--o~l9) -O.lj(-0.10)
-0.3j(-0.38) -0.03( -0.1 1) -O?j(-0.33) -0.‘3(-0.6’) -0.X-0.20) -0.33(-0.28) -0.20(-0.19) --0.13(-0.1-t) -0.30(-O-20)
Mran = Std dev.=
-0.39 0.1 I
-0.29 0.20
-0.23 0.1-I
-0.17(-0.25) 0~10(0~12)
-0.2-t-0.26) 0.19(0.16)
--0.3
--I).7
IN
0.Y
-O.?O( ._O- 10) ._@02( ._($Oz) -1).03( -0.13) _0.29(__0.30) __O.l+O.3l) -O.J7(-0.28) --0.08(_.0.10) _0.12(__O.l3) _ ().21(~_O.‘j)
-0.X( ~-o-lz) - O.O’( - 0.04) O.OO( O.(N) ~~0.2-h 0.2-I) 0.02( o-13)
0.04 O,UY u.u-1 0.07 0.06
-O.OY( 044) -0.02( 0.1I) -0.15( 0.13,
o-07
O-15( mO.lO)
0.02 0.10 0.22
--l).l6(~~O.l~) 0~10(0~1 I)
~ll.1-Q 0.1-I) 0. I j(O. I I )
0.07 047
Each value in the table is the mean PA ratio for a given subject in 4 to 6 trials at the indicated
illumlnance
le\sl.
analysis of variance (DIXONand MASSEY, 1951) indicates the regression curve is probably a straight line (5 per cent level of significance). In the retest series (Table 2. values in parentheses), wherein four retinal illuminances occurred in ascending order of magnitude, the regression coefficient is -0.13. Statistical significance of the regression coefficient for these retest values, however, is less than that for the initial test series (5 per cent vs. 0.5 per cent)-perhaps, because only half as much data was available for the retest series as for the initial series. The data were also examined for possibly significant changes in accommodative response with retinal illuminance. A small, but statistically significant (1 per cent level). average reduction in accommodative response with retinal illuminance was indeed evident for the nine subjects under discussion, and the minimum average accommodative response was 1.0 D f 0.24 at the lowest illuminance level (Table 3). One of the remaining two subjects (J.E.D.), showed essentially the same type of relationship as the preceding nine except that his ratios were much higher than those of the others (Table 4). Moreover, pupil constriction in this subject diminished at an average rate of TABLE 3. ACCOMMODATIVE
RESPONSESAT 8 RETINAL ILLUSIINASCELEVELS FOR THE SLXJFCTSOF T-\BLE2. RETEST VALUES ARE SHOW IN P.%RENTHESES Log trolands 0
-0.3
--0.7
0.9
I.1
0.8
0.j
0.2
T.B. A.De. .4.F. A.D.G. C.G. P.J.H. L.L. G.M. J.W.
l-2 I.3 I .-I I.2 I.0 I.1 1.3 I.8 0.9
0.9 1.4 1.j I.1 0.9 I.7 I.3 I.3 I.3
0.9 I.3 I ..l 1.1 I.0 I.0 I ,1 I.-t I.2
0.8(0.9) i.Z(l.3) 1.3(1,1) 1.2(1.3) 0.9( 1.0) l.Z(l.3) 1.2(1.2) I.I(l.J) I .O( I ,O)
0.q 1.0) 1.1(1.1) l.l(l.3) l.l(l.2) 0.9(0.9) 1,3(1.5) l.O(l.2) I.j(l.8) l’l(O.9) -
I .O( I .O) I .O( 1’ I ) 1.3(1.4) I-l(l.0) 0,9(0.9) l.Z(l.3) l-2(1.2) l.-I(I.S) l.I(I.1)
0.8( I .O) i~I(I~I) l.‘(I.I) I -O(0.9) I.O(l.0) 1.3(M) I.3(l.l) l.3(l.j) I ,O(O.Y)
0.6 0.9
Mean= Std dev. =
1.1s 0.26
I.26 0.26
I.19 0.20
1.13(1.19) 0,19(0.18)
I.1 l(l.21) 0.21(0.29)
l.l3(1.20) 0.16(0.27)
I.1 l(l.10) O.lS(O.21,
I.01 0.24
Each value in the table is the mean accommodative illuminance level.
response
_
for a given subject
IFI
I.1 u.9 0.9 l-3 I.-l 0.9
in 4 to 6 trials at the indicated
Effect of Reduced Retinal Illuminance on the Fupillary Near Reflex
1263
N~LE~ROTH
126-t
0.39 mm,‘diop/‘log unit, compared with about one third this value in the preceding nine (Table 2). Data from the last subject (A.Di.) also showed decreased PA ratios with retina1 illuminance, but here the ratios quickly decreased to values close to zero for six of the eight illuminance levels (Table 4). Furthermore, at the lowest illuminance level, the average pupil response was a relatively large dilatation as the eye accommodated for near. This unusual finding cannot be considered significant in itself since it occurred in only one subject. It is probably consistent, however, with the observation that this subject’s PA ratios were so little different from zero at the majority of illuminances that extraneous factors were more likely than usual to exhibit significant influences on pupii size (LOWENSTEIN and LOEWENFELD,1962). DISCUSSION
AND
CONCLUSIONS Results of the present investigation support the hypothesis that, in general, the pupillary near reflex functions in accord with other mechanisms that enhance the sensitivity of the eye to reduced retinal illuminances, This “adaptation” of the pupillary near reflex is manifested by a significant average reduction in the magnitude of constriction associated with one diopter of accommodative response as retinal illuminance decreases. The average findings for the majority of subjects (9 of 11) indicate a reduction in the PA ratio with retinal illuminance of about 0.14 mm/dioptilog unit (std dev. = O-IO). This value agrees closely with that obtained in the retest series (Table 2), indicating that subject fatigue probably played no significant part in the relationship between PA ratio and retinal illuminance. As noted, the tenth subject (J.E.D.) showed the same trend as the preceding nine, differing only in the size of his PA ratio and in the average rate of change with respect to illuminance. In contrast to the above, the near pupil reflex of the last subject (A.Di.) appeared to be relatively inoperative at the seven lower illuminances. It is also noteworthy that this subject exhibited a much greater loss of accommodative response with illuminance than did the others (Table 4). Average accommodation at the highest illuminance was 0.9 D, which decreased to O-2 D at the lowest illuminance-a change three times as large as the average value observed in the nine subjects of Table 2. Thus, it is very likely that subject A.Di. had insu~cient accommodative response at the seven lower illuminances for near reflex pupillary constriction to be linearly related to accommodative response. Since the change in accommodative stimulus in this case was held at a constant 1.6 D, it appears this subject was more strongly affected than the others by “night presbyopia” (ALPERN and LARSON,1960). It is reasonable to conclude that PA ratio in 10 of the 11 subjects did not vary with accommodative response, since the latter was sufficiently large at all the employed illuminance levels for near reflex pupil constriction to be linearly related to accommodation. This condition of linearity is, of course, necessary for the ratio of pupil constriction to accommodative response to remain constant with accommodative level. With an average accommodation of 1-Oto 1.3 D, PA ratio must vary linearly with log retinal illuminance alone, at least for the two log unit illuminance range that inciudes the transition zone from photopia to mesopia. The foregoing conclusion is consistent with the evidence that nerve impulses controlling near reflex pupil constriction and those that bring about ciliary muscle contraction arise from separate areas in the midbrain and have separate efferent paths (LO’NENSTEIN and LOEWENFELD,1962).
Effect of Reduced Retinal Illuminance on the Pupiiiary Near Reflex rlcknowledgemenr-The course of this investigation.
author is indebted to Mr. J. Lamus
for unfailing assistance throughout
1265 the
REFERENCES ALPERN, M. and LARSOS, B. F. (1960). Vergence and accommodation. Rm. J. Ophthal. 49, 1140-I 119. DIXON,W. J. and MASSEY, F. J. (1951). Introduction to Sturisricul Annfysis, McGraw-Hill, New York.
FRY, G. A. (1945). The relation of pupil size to accommodation and convergence. Am. J. Optom. 22, I-15. KSOLL, H. A. (1949). Pupillary changes associated with accommodation and convergence. Am. J. Optom. 27, 346-357. LEGRA?JD,Y. (1957). Light, Colow, and Vision, Chapman and Hall, London. LOWENSTEIN, 0. and LOEWE~FELD, I. E. (1962). The Eye. Muculur ~~ee~un~rn~(edited by H. DAVX~?~‘), Vol. 3, Academic Press, New York. M~RG, E. and MORGAN, M. W., JR. (1949). The pupillary near reflex. Am. J. Optom. 26, 183-197. IMARG,E. and MORGAZI,M. W., JR. (1950). Further investigation of the pupillary near reflex. Am. J. Opfom. 27, 217-225. ROTH, N. (1965). Automatic optometer for use with the undrugged human eye. Rev. scient. Instrum. 36, 16361641. ROTH,N. (1966). Startling noise and resting refractive state. Br. 1. Physiol. Opr. 23, 223-231. TSCHERMAK-SEYSENEGG, A. V. (1952). Introducrion to Physiologicui Optics. Charles C Thomas, Springfield, Illinois. APPENDIX An additional view of relations between the pupillary near reflex and comparison between initial and final pupil diameters at the eight retinal experiment. This treatment contrasts with the use of the PA ratio in that decreasing influence of accommodation on final pupil diameter as retinal
retinal illuminance is provided by a iliuminan~ levels employed in the it gives a more direct picture of the iiluminance is lowered (Fig. 2).
go$
7.0-
0 0
E
6.8 -
t, I <
6.6 -
l
l
0
0 0
*
0
0
0 o
z & 6.4 n. z
a
a 0
o
Initial Diom. Final Diom.
0 0
6.2 I -0.4
I
-0.7
I
-0.3
I
I
I
I
I
0
0.2
0.5
0.8
I.t
LOG RETtNAL ILLUMINANCE (TROLANDS) FIG. 2. Initial and final pupil diameters for the nine subjects of Table 2, Abstract-Changes in pupil diameter associated with a eonstant change in accomodative stimulus were measured as retinal iliuminance was varied over a range of two log units (troiands). In 10 of 11 subjects the magnitude of pupil constriction associated with one diopter of accomodative response decreased significantly as retinal illuminance dropped. This finding indicates that the near reflex pupillary response is directly related in magnitude to the existing level of illuminance and functions in accord with other adaptive mechanisms that alter the overall sensitivity of the eye. R~um&On mesure les variations du diambre pupitlaire associies a un changement constant du stimuhts accommodate en fonction de l’ecclairement r&in& qui varie dans un intervaile de deux unites Iogarithmiques (trolands). Sur 10 des I1 sujets la valeur de la constriction pupillaire associb a une dioptrie de riponse accommodative diminue dune facon significative quand I’ecelairement retinien baisse. Ce r&hat indique que la rtponse du riflexe pupillaire en vision de prts varie en grandeur avec le niveau actuel de luminance et fonctionne en accord avec d’autres mecanismes adaptatifs qui modifient la sensibilite globale de l’oeil.
1366
NILE ROTH
Zusammenfassuog-PPupillendurchmesserver8nderungen, die durch eine konstante Anderung des Akkommodationsreizes bedingt waren, wurden im Laufe von Netzhautbeleuchtungsverinderungen van 2 logarithmischen Einheiten (Troland) gemessen. Von elf untersuchten Subjekten zeigten zehn eine durch eine akkommodative Antwort einer Dioptrie bedingte Pupillenveranderung, welche sich deutlich mit der Netzhautbeleuchtung verringerte. Dies zeigt, dass sich der Nahretlex der Pupille seiner GrSsse nach an die bestehende Adaptierungslage koppelt und im Einklang mit anderen adaptiven Mechanismen, welche die gesamte Augenemp6ndlichkeit Bndern, wirkt. Pe3iome - IjblJIH ii3MePeHbl u3MeHeHNR B nEP.leTpe 3paYKa, CBI13aHHble C nOCTOWHbIM N3MeHeHUeM pa3fipaXQiTeJlR, K KOTOpOMy aKKO,MOAupyeT rfla3, npu TOM yCJlOBkiH,ST0 OCBeIIJeHHOCTb BapuupOBaIIaCb B npene;raX AByX nOrapu@MuWCKuX eLWHH4 (TpOJlaHLIOB).Y ,LWATu u3 OmHHaWaTIi uCl-lbITye,MbIX BeJIH%fHa CyxeHWl 3pa’fKa, CBI13aHHal C peaKlINen aKKOMOJlaUIiu COOTSeTCTByIOlUefi 0aHOi-iRuOnTpuu, npu yMeHbIUeHHH OCBeIIJeHHOCTu CeT'iaTKu 3Ha'4uTeJlbHO yMeHbUIajlaCb. 3TO Ha6ntonetrue yKa3bmaeT Ha ~0, 'ITO 3parKoebGi pe@neec npu npu6nHmeHHw paccMaTpunaeMOrO of&ma npnM0 CBR3aH cBenuwHo8 uMem.UerocR ~POBHR OCBeLLteHHOCTu n 3Ta 4yHmuIII: HaxomiTcfl B cornacuu c ApyrnMnMexaHu3m_vuaaLlanTauuw, KoTopble HSMeHIIIOT 06111ym 'IyBCTBUTeJIbHOCTb rIla3a.
Rtir.
Vol. 9. pp. 1159-I266
Pcrgamoo
Press
1969.
Pnnted in Great Britain.
EFFECT OF REDUCED RETINAL ILLUMINANCE ON THE PUPILLARY NEAR REFLEX1 NILES ROTH Jules Stein Eye Institute, Department of Ophthalmology, UCLA School of Medicine, Los Angeles, California 90024 (Received 5
March
1969)
INTRODUCTION PUPILLARY constriction that occurs when a normal observer changes fixation from far to near has been studied by a number of investigators with a view to determining possible relations to accommodation and the various components of convergence (FRY, 1945; MARC and MORGAN, 1949, 1950; KNOLL, 1949). MARG and MORGAN (1950) concluded that, under normal conditions, the pupillary near reflex is elicited principally by accommodation with fusional convergence playing a minor role in some subjects and none at all in others. Moreover, pupillary diameter as a function of accommodation was found to be linear, although in some cases, only after about the hrst diopter of accommodative response. In general, the findings of Marg and Morgan agree with those of Knoll. An additional aspect of near reflex pupillary constriction and accommodation that will be considered here is the effect of reduction of retinal illuminance on the quantitative relationship between these two functions. As the retina adapts to lower illuminance levels, pupil size increases, provided the accommodative levels remain constant (LE GRAND, 1957). Thus, at photopic levels in the accommodating eye, pupil constriction associated with increased neural stimulation of the ciliary muscle and pupil dilation accompanying reduced retinal illuminance antagonize each other. Although it is recognized that the adverse influence of spherical aberration on retinal image becomes more serious as the pupil dilates, the traditional view is that maintenance of image clarity becomes secondary to attainment of maximum sensitivity as illumination levels drop below photopia. Thus, a larger pupil is more advantageous at reduced illuminances because more of the available light is collected. If the above view is correct, the ratio of change in pupil size to change in accommodation would be expected to diminish at lower illuminance levels, so there would be as little interference as possible with the collecting of quanta by the eye. The purpose of this study was to determine whether the relationship between pupil constriction and accommodation does indeed vary significantly as a function of retinal illuminance when. the latter is altered over a range that includes the transition zone between photopia and mesopia. MATERIALS
AND METHODS
Simultaneous records of accommodative response and pupil means of an automatic optometer with pupillograph attachment. records of refractive change that are not influenced by variations greater than 4.5 mm. Conversely, the pupillographic information,
size change, in the same eye, were obtained by This device is capable of providing continuous in pupil size, provided pupa diameter remains consisting of oscillograph records and infrared
t This investigation was supported by a PHS Research Grant NB-2709 from the National Institute of Neurological Diseases and Blindness, Bethesda, Maryland. 1259
NiLEs RorH
I160
pupil photographs, is not affected by changes in ocular refractive power (ROTH. 1965). Under normal viewing conditions, retinal illuminance is influenced by fluctuations in pupil size. Thus. as mentioned eariier, when the pupil constricts with a change in fixation from far to near. pupiltary light response opposes near reflex constriction with compensatory dilation. Therefore, if the aim is to study the pupillary near reflex as separate from the light retfex, the accommodative stimulus must be controlled in the laboratory, SO that retinal iliuminance is independent of pupil size. MARG and iMORCAZi (1949) avoided interaction between the light and near reflexes of the pupil by adjusting the target luminance at each fixation distance for a standard flicker rate. Thus, they maintained, a constant retinal illuminance for all fixation distances and pupil size variations occurring with changes in fixation distance could be ascribed to factors separate from the pupillary light response. The present investigation utilized a different means of avoiding interaction between light and near reflexss of the pupil. This consisted of an optical system in which the target was seen through an exit pupil, 3 mm in dia., centered around the visual axis and located in the plane of the entrance pupil of the test eye (ROTH, 1966). The minimum natural pupil diameter for ail subjects was always considerably greater than the diameter of the exit pupil of the accommodative stimulus system. so that retinal illuminance remained constant over the range of pupil diameters encountered in this experiment. Target luminance was controlled with neutral filters (ROTH. 1966). Luminance levels ranged from 5.6 x l@t to 5.2 x 10-J miliilamberts (mL).Z When these tuminances are compared with the ievel corresponding to the transition from photopia to mesopia (3 x IO-2 mL, Tschermak), it is seen that five test luminances fall above the upper limit for twilight vision and three below this limit (Table 1). TABLE1, &TlYAL A CONSTANT
ILLUMINANCE
VS. TARGET
LUMINANCE
EFFECTIVE PUPIL DIAMETER OF
3 mm
FOR
(AREA=
7.07 mmz) Target luminance (mL) 0.56
0.28 0.13 0.06 I 0.045 0.023 0.0097 O,OOE
Retinal illuminance Log trolands Trolands (to nearest tenth) 12.6 6.3 2.9 1.4 1.0 0.52 0.22 0.12
1.1 0.8 0.5 0.2 0 -0.3 -0.7 -0.9
Troland values were calculated as follows: Trolands = (mL) (3.18)*(7.07 mmr). * Conversion factor, mL to cd/m’-. Limitations in the apparatus made it impractica1 to correct the subject’s refractive error during the course of the experiment, but near and far target locations coutd be chosen to elicit adequate accommodation for studying near response of the pupil. Excessive accommodation had to be avoided. as it would have been accompanied by pupil diameters smaller than the 4.5 mm minimum demanded by the present methods of measurement. The eleven research subjects of this experiment were male students at the University of California, Los Angeles, ranging in age from 18 to 28 yr. All had prior training with the same apparatus in this laboratory during an earlier experiment (ROTH, 1966): in the present experiment, the subjects participated in a total of 60 trials with two or three day intervafs between trials for a given subject. The accommodative stimulus targets (2-degree field) have been described elsewhere (ROTH, 1965). The experimental procedure
Target luminance was set at 0.56 mL (highest level), and the subject’s eye was aligned in the apparatus. The left eye was occluded and two targets were chosen for the right eye so that approximately one diopter of accommodative response would be elicited on changing fixation from the far target to the near one. Adaptation to the existing illuminance level was determined by observing the pupillographic record as the subject fixated the far target. As soon as a relatively constant pupil diameter was indicated by minimum fluctuation of the pupillographic tracing. the subject was instructed to signal with a buzzer that the target was * Values derived from measurements photometer.
made with a UB-l-I/2
Photoresearch
Corporation
photoelectric
Effect of Reduced Retina! Illuminance on the Pupillary Near Reflex
1261
seen clearly. Following this signal, a pupil photograph was taken, the far target was replaced with the near one, the subject signaled again when he saw the target clearly, a second photograph was taken, the far target was restored. and the test sequence ended with a final signal from the subject that the far target was seen clearly. The foregoing six occurrences, spanning an interval of about 10 set, were recorded by the event marker of a pen recorder that also recorded in separate channels simultaneous accommodative and pupillary responses on the same time base. Infrared photographs were measured later and pupil size data inserted into the record at positions on the time scale indicated by the appropriate event marks (Fig. 1).
2
L
FIG. 1. Simultaneous records of accommodative response (I) and relative pupil area (2). Marks in event trace (E) indicate: B,-subject’s signal that far target is clear; P,-camera shutter open for first pupil photograph; N-near target in view; Ba-signal that near target is seen clearly; P?-camera shutter open for second pupil photograph; BsYsigna! that far target is seen clearly. Remaining equally spaced marks in trace E indicate I-set intervals. Figures above pupillograph trace (2) show pupil diameters (mm) obtained later by measuring pupil photographs. The above described procedure was carried out for eight different target luminances in descending order of magnitude. Four additional (retest) sequences were conducted by repeating, in ascending order of magnitude, tests with the four levels above the lowest one. Thus, a total of 12 test sequences were run in each trial, using eight luminance levels. The additional four tests were intended to reveal any fatigue effects that might have influenced the relationship between accommodation and near reflex pupillary constriction at the lowest retina! illuminances. In the preliminary design of the experiment, presentation of target luminances in random order of magnitude was considered and later rejected; experience showed that if the trial duration exceeded a half hour, unstable records resulted from most subjects. Random presentation would have required that the subject adapt to occasional markedly different retina! illuminance levels from ‘one sequence to the next. The additional time needed by the subject to adapt to these large illuminance changes might have introduced the risk of instability in the records. RESULTS
At each retinal illuminance level, relationships between near reflex pupil constriction and accommodation are shown by the ratio of average change in pupil diameter (mm) to average simultaneous change in accommodative level (diopt). For convenience, this quotient is designated “PA ratio” (KNOLL, 1949). Data from 9 of the 11 subjects appeared similar enough to suggest composite treatment of the results (Table 2). Part of the variability in PA ratio at each retinal illuminance level is probably due to influences that are separate from either retinal illuminance or accommodation (LOWENSTEIN and LOEWENFELD, 1962). The two remaining subjects will be considered separately. The data of Table 2 (9 subjects) were analyzed with respect to significance and linearity of the relationship between PA ratio and retinal illuminance. The estimated mean slope of the regression curve of PA ratio on log trolands is -0.14; i.e. the change in pupil diameter associated with one diopter of accommodation diminishes at an average rate of about 0.14 mm per log unit as retinal illuminance decreases. This reduction in PA ratio is statistically significant at the 0.5 per cent level and a test of the linearity of regression by
NILES ROTH
1261
TABLE 2. PA RATIOS AT 8 RETINAL ILLIMINANCE LEVELS FOR 9 SUBJECTS. RETEST \.ALUESARE SHOWN PARENTHESES
I.1
0.8
0.j
0.2
Log trolands 0
T.B. A.De. A.F. A.D.G C.G. P.J.H. L.L. G.M. J.W.
-0.16 -0.32 -O.jl -0.M -0.j3 -0.10 -0.29 -0.16 -0.u
PO.37 -0.07 -0.09 -0.29 -0.69 -O.-l1 -0.x -0.12 -0.25
-0.37 -0.03 --0.45 -0.34 -0.12 --0.10 --0.16 -0.11 -0.2j
-0~35(-0~25) -0.02( -0.08) -O.lj(-0.19) -O.l7(-0.38) -0.2-I-O.lj) -0.20(-0.10) -O-14(-0.17) -o~lo(--o~l9) -O.lj(-0.10)
-0.3j(-0.38) -0.03( -0.1 1) -O?j(-0.33) -0.‘3(-0.6’) -0.X-0.20) -0.33(-0.28) -0.20(-0.19) --0.13(-0.1-t) -0.30(-O-20)
Mran = Std dev.=
-0.39 0.1 I
-0.29 0.20
-0.23 0.1-I
-0.17(-0.25) 0~10(0~12)
-0.2-t-0.26) 0.19(0.16)
--0.3
--I).7
IN
0.Y
-O.?O( ._O- 10) ._@02( ._($Oz) -1).03( -0.13) _0.29(__0.30) __O.l+O.3l) -O.J7(-0.28) --0.08(_.0.10) _0.12(__O.l3) _ ().21(~_O.‘j)
-0.X( ~-o-lz) - O.O’( - 0.04) O.OO( O.(N) ~~0.2-h 0.2-I) 0.02( o-13)
0.04 O,UY u.u-1 0.07 0.06
-O.OY( 044) -0.02( 0.1I) -0.15( 0.13,
o-07
O-15( mO.lO)
0.02 0.10 0.22
--l).l6(~~O.l~) 0~10(0~1 I)
~ll.1-Q 0.1-I) 0. I j(O. I I )
0.07 047
Each value in the table is the mean PA ratio for a given subject in 4 to 6 trials at the indicated
illumlnance
le\sl.
analysis of variance (DIXONand MASSEY, 1951) indicates the regression curve is probably a straight line (5 per cent level of significance). In the retest series (Table 2. values in parentheses), wherein four retinal illuminances occurred in ascending order of magnitude, the regression coefficient is -0.13. Statistical significance of the regression coefficient for these retest values, however, is less than that for the initial test series (5 per cent vs. 0.5 per cent)-perhaps, because only half as much data was available for the retest series as for the initial series. The data were also examined for possibly significant changes in accommodative response with retinal illuminance. A small, but statistically significant (1 per cent level). average reduction in accommodative response with retinal illuminance was indeed evident for the nine subjects under discussion, and the minimum average accommodative response was 1.0 D f 0.24 at the lowest illuminance level (Table 3). One of the remaining two subjects (J.E.D.), showed essentially the same type of relationship as the preceding nine except that his ratios were much higher than those of the others (Table 4). Moreover, pupil constriction in this subject diminished at an average rate of TABLE 3. ACCOMMODATIVE
RESPONSESAT 8 RETINAL ILLUSIINASCELEVELS FOR THE SLXJFCTSOF T-\BLE2. RETEST VALUES ARE SHOW IN P.%RENTHESES Log trolands 0
-0.3
--0.7
0.9
I.1
0.8
0.j
0.2
T.B. A.De. .4.F. A.D.G. C.G. P.J.H. L.L. G.M. J.W.
l-2 I.3 I .-I I.2 I.0 I.1 1.3 I.8 0.9
0.9 1.4 1.j I.1 0.9 I.7 I.3 I.3 I.3
0.9 I.3 I ..l 1.1 I.0 I.0 I ,1 I.-t I.2
0.8(0.9) i.Z(l.3) 1.3(1,1) 1.2(1.3) 0.9( 1.0) l.Z(l.3) 1.2(1.2) I.I(l.J) I .O( I ,O)
0.q 1.0) 1.1(1.1) l.l(l.3) l.l(l.2) 0.9(0.9) 1,3(1.5) l.O(l.2) I.j(l.8) l’l(O.9) -
I .O( I .O) I .O( 1’ I ) 1.3(1.4) I-l(l.0) 0,9(0.9) l.Z(l.3) l-2(1.2) l.-I(I.S) l.I(I.1)
0.8( I .O) i~I(I~I) l.‘(I.I) I -O(0.9) I.O(l.0) 1.3(M) I.3(l.l) l.3(l.j) I ,O(O.Y)
0.6 0.9
Mean= Std dev. =
1.1s 0.26
I.26 0.26
I.19 0.20
1.13(1.19) 0,19(0.18)
I.1 l(l.21) 0.21(0.29)
l.l3(1.20) 0.16(0.27)
I.1 l(l.10) O.lS(O.21,
I.01 0.24
Each value in the table is the mean accommodative illuminance level.
response
_
for a given subject
IFI
I.1 u.9 0.9 l-3 I.-l 0.9
in 4 to 6 trials at the indicated
Effect of Reduced Retinal Illuminance on the Fupillary Near Reflex
1263
N~LE~ROTH
126-t
0.39 mm,‘diop/‘log unit, compared with about one third this value in the preceding nine (Table 2). Data from the last subject (A.Di.) also showed decreased PA ratios with retina1 illuminance, but here the ratios quickly decreased to values close to zero for six of the eight illuminance levels (Table 4). Furthermore, at the lowest illuminance level, the average pupil response was a relatively large dilatation as the eye accommodated for near. This unusual finding cannot be considered significant in itself since it occurred in only one subject. It is probably consistent, however, with the observation that this subject’s PA ratios were so little different from zero at the majority of illuminances that extraneous factors were more likely than usual to exhibit significant influences on pupii size (LOWENSTEIN and LOEWENFELD,1962). DISCUSSION
AND
CONCLUSIONS Results of the present investigation support the hypothesis that, in general, the pupillary near reflex functions in accord with other mechanisms that enhance the sensitivity of the eye to reduced retinal illuminances, This “adaptation” of the pupillary near reflex is manifested by a significant average reduction in the magnitude of constriction associated with one diopter of accommodative response as retinal illuminance decreases. The average findings for the majority of subjects (9 of 11) indicate a reduction in the PA ratio with retinal illuminance of about 0.14 mm/dioptilog unit (std dev. = O-IO). This value agrees closely with that obtained in the retest series (Table 2), indicating that subject fatigue probably played no significant part in the relationship between PA ratio and retinal illuminance. As noted, the tenth subject (J.E.D.) showed the same trend as the preceding nine, differing only in the size of his PA ratio and in the average rate of change with respect to illuminance. In contrast to the above, the near pupil reflex of the last subject (A.Di.) appeared to be relatively inoperative at the seven lower illuminances. It is also noteworthy that this subject exhibited a much greater loss of accommodative response with illuminance than did the others (Table 4). Average accommodation at the highest illuminance was 0.9 D, which decreased to O-2 D at the lowest illuminance-a change three times as large as the average value observed in the nine subjects of Table 2. Thus, it is very likely that subject A.Di. had insu~cient accommodative response at the seven lower illuminances for near reflex pupillary constriction to be linearly related to accommodative response. Since the change in accommodative stimulus in this case was held at a constant 1.6 D, it appears this subject was more strongly affected than the others by “night presbyopia” (ALPERN and LARSON,1960). It is reasonable to conclude that PA ratio in 10 of the 11 subjects did not vary with accommodative response, since the latter was sufficiently large at all the employed illuminance levels for near reflex pupil constriction to be linearly related to accommodation. This condition of linearity is, of course, necessary for the ratio of pupil constriction to accommodative response to remain constant with accommodative level. With an average accommodation of 1-Oto 1.3 D, PA ratio must vary linearly with log retinal illuminance alone, at least for the two log unit illuminance range that inciudes the transition zone from photopia to mesopia. The foregoing conclusion is consistent with the evidence that nerve impulses controlling near reflex pupil constriction and those that bring about ciliary muscle contraction arise from separate areas in the midbrain and have separate efferent paths (LO’NENSTEIN and LOEWENFELD,1962).
Effect of Reduced Retinal Illuminance on the Pupiiiary Near Reflex rlcknowledgemenr-The course of this investigation.
author is indebted to Mr. J. Lamus
for unfailing assistance throughout
1265 the
REFERENCES ALPERN, M. and LARSOS, B. F. (1960). Vergence and accommodation. Rm. J. Ophthal. 49, 1140-I 119. DIXON,W. J. and MASSEY, F. J. (1951). Introduction to Sturisricul Annfysis, McGraw-Hill, New York.
FRY, G. A. (1945). The relation of pupil size to accommodation and convergence. Am. J. Optom. 22, I-15. KSOLL, H. A. (1949). Pupillary changes associated with accommodation and convergence. Am. J. Optom. 27, 346-357. LEGRA?JD,Y. (1957). Light, Colow, and Vision, Chapman and Hall, London. LOWENSTEIN, 0. and LOEWE~FELD, I. E. (1962). The Eye. Muculur ~~ee~un~rn~(edited by H. DAVX~?~‘), Vol. 3, Academic Press, New York. M~RG, E. and MORGAN, M. W., JR. (1949). The pupillary near reflex. Am. J. Optom. 26, 183-197. IMARG,E. and MORGAZI,M. W., JR. (1950). Further investigation of the pupillary near reflex. Am. J. Opfom. 27, 217-225. ROTH, N. (1965). Automatic optometer for use with the undrugged human eye. Rev. scient. Instrum. 36, 16361641. ROTH,N. (1966). Startling noise and resting refractive state. Br. 1. Physiol. Opr. 23, 223-231. TSCHERMAK-SEYSENEGG, A. V. (1952). Introducrion to Physiologicui Optics. Charles C Thomas, Springfield, Illinois. APPENDIX An additional view of relations between the pupillary near reflex and comparison between initial and final pupil diameters at the eight retinal experiment. This treatment contrasts with the use of the PA ratio in that decreasing influence of accommodation on final pupil diameter as retinal
retinal illuminance is provided by a iliuminan~ levels employed in the it gives a more direct picture of the iiluminance is lowered (Fig. 2).
go$
7.0-
0 0
E
6.8 -
t, I <
6.6 -
l
l
0
0 0
*
0
0
0 o
z & 6.4 n. z
a
a 0
o
Initial Diom. Final Diom.
0 0
6.2 I -0.4
I
-0.7
I
-0.3
I
I
I
I
I
0
0.2
0.5
0.8
I.t
LOG RETtNAL ILLUMINANCE (TROLANDS) FIG. 2. Initial and final pupil diameters for the nine subjects of Table 2, Abstract-Changes in pupil diameter associated with a eonstant change in accomodative stimulus were measured as retinal iliuminance was varied over a range of two log units (troiands). In 10 of 11 subjects the magnitude of pupil constriction associated with one diopter of accomodative response decreased significantly as retinal illuminance dropped. This finding indicates that the near reflex pupillary response is directly related in magnitude to the existing level of illuminance and functions in accord with other adaptive mechanisms that alter the overall sensitivity of the eye. R~um&On mesure les variations du diambre pupitlaire associies a un changement constant du stimuhts accommodate en fonction de l’ecclairement r&in& qui varie dans un intervaile de deux unites Iogarithmiques (trolands). Sur 10 des I1 sujets la valeur de la constriction pupillaire associb a une dioptrie de riponse accommodative diminue dune facon significative quand I’ecelairement retinien baisse. Ce r&hat indique que la rtponse du riflexe pupillaire en vision de prts varie en grandeur avec le niveau actuel de luminance et fonctionne en accord avec d’autres mecanismes adaptatifs qui modifient la sensibilite globale de l’oeil.
1366
NILE ROTH
Zusammenfassuog-PPupillendurchmesserver8nderungen, die durch eine konstante Anderung des Akkommodationsreizes bedingt waren, wurden im Laufe von Netzhautbeleuchtungsverinderungen van 2 logarithmischen Einheiten (Troland) gemessen. Von elf untersuchten Subjekten zeigten zehn eine durch eine akkommodative Antwort einer Dioptrie bedingte Pupillenveranderung, welche sich deutlich mit der Netzhautbeleuchtung verringerte. Dies zeigt, dass sich der Nahretlex der Pupille seiner GrSsse nach an die bestehende Adaptierungslage koppelt und im Einklang mit anderen adaptiven Mechanismen, welche die gesamte Augenemp6ndlichkeit Bndern, wirkt. Pe3iome - IjblJIH ii3MePeHbl u3MeHeHNR B nEP.leTpe 3paYKa, CBI13aHHble C nOCTOWHbIM N3MeHeHUeM pa3fipaXQiTeJlR, K KOTOpOMy aKKO,MOAupyeT rfla3, npu TOM yCJlOBkiH,ST0 OCBeIIJeHHOCTb BapuupOBaIIaCb B npene;raX AByX nOrapu@MuWCKuX eLWHH4 (TpOJlaHLIOB).Y ,LWATu u3 OmHHaWaTIi uCl-lbITye,MbIX BeJIH%fHa CyxeHWl 3pa’fKa, CBI13aHHal C peaKlINen aKKOMOJlaUIiu COOTSeTCTByIOlUefi 0aHOi-iRuOnTpuu, npu yMeHbIUeHHH OCBeIIJeHHOCTu CeT'iaTKu 3Ha'4uTeJlbHO yMeHbUIajlaCb. 3TO Ha6ntonetrue yKa3bmaeT Ha ~0, 'ITO 3parKoebGi pe@neec npu npu6nHmeHHw paccMaTpunaeMOrO of&ma npnM0 CBR3aH cBenuwHo8 uMem.UerocR ~POBHR OCBeLLteHHOCTu n 3Ta 4yHmuIII: HaxomiTcfl B cornacuu c ApyrnMnMexaHu3m_vuaaLlanTauuw, KoTopble HSMeHIIIOT 06111ym 'IyBCTBUTeJIbHOCTb rIla3a.