May 1966

JOURNAL OF THE OPTICAL SOCIETY OF AMERICA VOLUME 56, NUMBER 5

Analysis of Photopic and Scotopic Function in an Incomplete Achromat*

IRWIN M. SIEGEL, CLARENCE H. GRAHAM, HARRIS Ripps, AND YuN HsIADepartment of Ophthalmology, NVew York University Medical Center, New York, New York 10016

andDepartment of Psychology, Columbia University, New York, New York 10027

(Received 11 August 1965)

Spectral sensitivity and color vision tests were performed on a subject who was totally color blind at lowphotopic luminances, but exhibited hue discrimination at relatively high photopic levels. Chromaticityconfusion loci showed that the residual color vision was abnormal; a tritan defect was superimposed on thegeneralized reduction of cone sensitivity. Although cone function was markedly depressed, a photopicspectral sensitivity curve was obtained for the light-adapted fovea. Dark-adapted foveal measurements, onthe other hand, gave a scotopic function almost identical to that of the dark-adapted periphery. However,it was possible to demonstrate objectively that this subject shifts fixation to an eccentric position underscotopic conditions, i.e., the dark-adapted "foveal" results were, in fact, for a para-macular region. Ir-respective of the degree of light adaptation, cone function was not detectable in the peripheral measurements.INDEX HEADINGS: Vision; Color vision.

TYPICAL achromatopsia (rod monochromacy) ischaracterized by total color blindness, poor visual

acuity, and an aversion to bright light; nystagmus isusually present in infancy, but gradually becomes lessapparent or disappears. These symptoms seem to resultfrom absence, or dysfunction, of the normal photopic(cone) mechanism. 1' 2 A less severe form of the conditionalso occurs in which there is rudimentary color discrimi-nation and somewhat better acuity.2-4 This defect isreferred to as incomplete or atypical achromatopsiasince the residual color vision is often manifest only atspecific luminances and not throughout the photopicrange.

Adaptometric, electroretinographic, and spectral sen-sitivity studies have demonstrated that the incompleteachromat has normal scotopic (rod) function, but mark-edly defective photopic vision. Some of the findings

* Work supported by Grants B-2589, NB-05487, and NB-18,766of The National Institute of Neurological Diseases and Blindness,U. S. Public Health Service, and by Contract Nonr 266(46) be-tween Columbia University and the Office of Naval Research.The document is Technical Report No. 35 of that contract. Thework is part of the program of Project NR 142-404. It has projectnumber PN 35. Reproduction in whole or in part is permitted forany purpose of the United States government.

I R. Harrison, D. Hoefnagel, and J. N. Hayward, Arch. Oph-thalmol. 64, 685 (1960).

2 G. Goodman, H. Ripps, and I. M. Siegel, Arch. Ophthalmol.70, 214 (1963).

L. L. Sloan, J. Opt. Soc. Am. 44, 117 (1954).H. R. Blackwell and 0. M. Blackwell, Vision Res. 1, 62 (1961).

suggest that these subjects exhibit rod as well as coneactivity in the fovea, the rod-free region of the normalretina.3' 4 But valid interpretation of such data requiresa means of determining the subject's fixation abilityin the various test situations. As regards the spectralresponsiveness of the defective cone mechanism, anoma-lous color discrimination has been reported, but theresponses were not considered indicative of a particularcategory of color defect.2' 3

The present report is based on an extensive study ofvisual function in an incomplete achromat. To explorethe possibility that the level of illumination at whichthe color tests are administered influences the characterof the responses, testing was performed at several inten-sities. By using these manifold stimulus conditions inthe spectral sensitivity measurements and tests of colordiscrimination, we were better able to assess the relativecontributions of scotopic and photopic mechanisms tothe visual function of our subject. In addition, theaccuracy of fixation for the light-and dark-adapted eyewas determined photographically, thus providing acheck on the location of the retinal area stimulated dur-ing the various test procedures.

METHODS

Subjects

Three individuals with normal color vision served assubjects in addition to D.M., the incomplete achromat.

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AI

I,< C

FIG. 1. Score profiles of the Farnsworth-M1unsell 100-Hue Test.Subject: D. M. (A) 37 ft-c, illuminant C; (B) 125 ft-c, "daylight"fluorescent lamps; (C) 11 150 ft-c, direct sunlight.

The latter was a 20 year-old female who suffered poorvisual acuity, photophobia, and nystagmus from in-fancy. Abnormal color vision was noted in early child-hood. Her only sib, a younger sister, has almost iden-tical symptoms. Both children are offspring of a non-consanguinous marriage and no other members of thefamily are known to be similarly affected.

Routine ophthalmological examination of D.M. re-vealed a corrected visual acuity of about 20/150 in eacheye and normal perimetric fields. She exhibited an aver-sion to bright lights, but nystagmus was not manifestat this time. Irregular pigmentation (mottling) was seenin both macular regions ophthalmoscopically, and onlythe fovea of the right eye gave a discrete reflex. Outsidethe central region, the fundus appeared normal.

D.M. has served as subject for other studies and thefindings indicate that her peripheral retina functionsalmost exclusively as a scotopic system whereas herfovea has photopic elements identifiable physiologicallyas cones. Briefly, the evidence for this view stems fromthe following observations: (1) Dark adaptometry ofD.M.'s peripheral retina gave a monophasic curve withabsence of the photopic segment, but final scotopicthresholds were normal2 ' 5; (2) the electroretinogramshowed normal scotopic activity, but photopic responsesto intense flickering lights could not be elicited2' 5 ; (3)increment-threshold measurements6 in the fovea re-vealed the presence of photopic receptors whose spectralresponsiveness differed from that of the rod mechanism 7;and (4) the Stiles-Crawford effect could be demon-strated foveally, but not in the peripheral retina.7

Color Vision Tests

A. Sloan A cltroniatopsia Test3 and A.0.H-iR-R Pseudoisoclhromnatic Plates

The Sloan test (1963 Edition) consists of a series of17 Munsell grey fields (ranging from 1.0 to 9.0 on theNeutral Value Scale) and 6 high-chroma Munsell papers.The subject is required to match each of the high-

R. E. Carr and I. M. Siegel, Am. J. Ophthalmol. 58, 95 (1964).6 W. S. Stiles and B. H. Crawford, Proc. Roy. Soc. (London)

112B, 428 (1933).7 M. G. F. Fuortes, R. D. Gunkel, and W. A. H. Rushton, J.

Physiol. 156, 179 (1961).

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chroma strips (red, orange, . . . , purple) to one of thegrey values. A match indicates that the subject can notdistinguish the particular hue from grey.

Both the Sloan and A.O. H-R-R tests were performedat several levels of illumination by placing a Macbetheasel lamp (illuminant C) at various distances from thetest materials. The illuminances employed were 0.1, 0.4,0.6, 2.0, and 20 ft-c. One of the color-normal subjectswas examined under identical conditions to provide com-parison data.

B. Farnsworthl-Munsell 100-Hue Test8

This test consists of four panels of numbered Munsellchips varying in hue, but of equal saturation and bright-ness. The subject is required to arrange the chips inconsecutive color order between fixed terminal chips.Errors are accumulated when the steps between chipsordered by the subject are out of numerical sequence.Color defective subjects score most of their errors ona series of chips whose colors fall in regions of the spec-trum which to them appear desaturated. Thus, on theprofile-scoring sheet, protan, deutan, and tritan accumu-late errors along different axes.8

D.Mi. was given the Farnsworth-Munsell 100-HueTest under three different levels of illumination: 37 ft-c(Macbeth Illuminant C), 125 ft-c (daylight fluorescentlamps), and 11 150 ft-c (direct sunlight).

C. ChIromaticity Confusion Loci

Dichromats can be classified according to theirchromaticity confusions by use of the Farnsworth-Munsell 100-Hue Test materials.9"l0 The examiner se-lects, at random, chips from each of the four panels inturn and the subject is asked to choose a matching chipfrom one of the remaining panels. In this way, severalpairs are obtained which appear alike to the dichromat.Since the xy coordinates on the CIE chromaticity dia-gram are known for each of the chips,1 ' the confusedcolors are referable to the normal chromaticity chart.The orientation of the lines formed by connecting thepoints on the diagram are diagnostic for a particulardichromatism. Chromaticitv confusion loci were estab-lished for D.M. under the same illumination conditionsused in the 100-Hue Test.

Spectral Sensitivity

A double monochromator provided the colored stimulifor the spectral-sensitivity determinations. The lightsource was a 6V 18A tungsten ribbon-filament lampoperated on direct current. The stimulus field was seen

8 D. Farnsworth, J. Opt. Soc. Am. 33, 568 (1943).9 G. Verriest (personal communication)."Y. Hsia and C. H. Graham, in Vision and Visual Perception,

C. H. Graham, Ed. (John Wiley & Sons, Inc., New York, 1965),Chap. 14.

W' W. C. Granville, D. Nickerson, and C. E. Foss, J. Opt. Soc.Am. 33, 376 (1943).

May 1966 LUMINOSITY FUNCTIONS IN INCOMPLETE ACHROMAT

0.4

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0.00.4 0.6 0.8 0.2 0.4X X

Y

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FIG. 2. Color-confusion lines for subject D. M. mapped on the CIE chromaticity diagram. Same illuminants as in Fig. 1.

in Maxwellian view, and subtended 42 min of arc at theeye. Single exposures of 4-msec duration were producedby a clutch-controlled slotted disk rotating on the shaftof a synchronous motor. A detailed description of theapparatus and its modification is given elsewhere."2'" 3

Threshold measurements of the dark-adapted foveawere obtained by having the subject fixate between twodim spots placed near the border of the test field. Forperipheral testing, the subject fixated a single spotlocated 70 nasal to the test field.

Increment thresholds were determined by superposingthe stimulus flash upon a white (50000K) rectangularsurround, 90 X40 in angular extent, which gave a con-stant background luminance of 0.55 mL. An additionalexperimental condition was used with subject D.M.:measurements of foveal thresholds with the light-adapt-ing background reduced to 0.055 mL.

Dark Adaptometry

A modified Goldmann-Weekers recording adaptom-eter was used to study the course of dark adaptation.Prior to each experimental session, the subject's pupilwas dilated with 10% neosynephrine and 1% Cyclogyl.The test was performed monocularly following an initial7 min exposure to 2800 mL. Measurements were madefor white light with a 10 test field located 100 belowfixation and, in a second experiment, with a 60 targetcentrally fixated.

RESULTS

The results of the Sloan Achromatopsia Test showedthat D.M. could match each of the six colored strips tosome grey value at all but the highest illuminance (20ft-c). The grey-match values chosen by our subject

12 S. Hecht, S. Shlaer, and M. Pirenne, J. Gen. Physiol. 25, 819(1942).

13 Y. Hsia and C. H. Graham, Proc. Natl. Acad. Sci. 38, 80(1952).

agree very well with those obtained by Sloan3 for a largegroup of typical achromats. Therefore, up to and in-cluding the 2 ft-c level she can be classified as an achro-mat. When the illuminance was increased to 20 ft-c,however, she could not match any of the Sloan Testcolors to grey. At this illuminance she was probably dis-criminating differences in chroma since, when asked,she named correctly most of the test colors. In contrast,Sloan's typical achromats continued to match all testcolors against grey at an illuminance of 37 ft-c. It shouldbe noted that a normal subject, tested under identicalconditions, readily distinguished the colored strips fromgrey even at the lowest illuminance.

Responses to the A.O. H-R-R plates were also ob-tained at the illuminances used in the Sloan Test. Ex-cept for an occasional plate in the more strongly satu-rated blue-yellow series (Nos. 19, 20) none of the figurescould be recognized until the illuminance reached 20ft-c. At this illuminance, the only other plates D.M.could identify correctly were the highly saturated red-green figures (Nos. 13 to 16).

Figure 1 shows score patterns of the Farnsworth-Munsell 100-Hue Test at three different test illumi-nances. With the standard Macbeth easel lamp (37ft-c), D.M. showed such poor hue discrimination that itwas necessary to plot her errors beyond the range of thescoring rings. When the test was given at 125 ft-c herhue discrimination showed some over-all improvement,with the major errors clustering around the opposingred and blue-green poles of the diagram. Under directsunlight, there was a shift from the general confusionin hue discrimination to a more clearly defined dichro-matic response. The accumulation of errors along thevertical axis of the scoring pattern indicates a tritandefect.

Further evidence that D.M. has a B-Y color defectis shown by the chromaticity confusion loci in Fig. 2.At low illuminances the family of lines shows a tendencyto converge on the violet corner of the CIE chromaticity

08

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7 SIEGLF., GRAHAM, RIPPS, ANT) HSISA

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FIG. 3. Spectral-sensitivity curves from central and peripheralretina of a normal observer, I.M.S. (e) Dark-adapted eye, 70nasal retina; (o) dark adapted, central retina; (3) light adaptedto 0.55 mL, 70 nasal retina; (c) light adapted to 0.55 mL, centralretina. Data obtained with a 42-min test field at an exposure dura-tion of 4 msec. The effective entrance pupil was 4 mm in diameter.

diagram. The convergence is far better at the twohighest illuminances and indicates the presence of atritanopic defect.54

p Figure 3 shows spectral-sensitivity functions for thecentral and peripheral retina of a normal subject. Twoother normal subjects gave similar results (not shown)except for some minor variations in the blue end of thespectrum. In plotting the data, the sensitivity maximaof the peripheral scotopic curves (i.e., the reciprocal ofthe energy required at the absolute threshold for , = 500mm) for the three normal observers were averaged andset at unity on the scale of ordinates. The individualdark- and light-adapted measurements, including thosefor achromat D.M. (Fig. 5), were plotted relative tothis value.

Spectral-sensitivity data (Fig. 4) for the dark-adaptedperipheral retina of D.M. are in good agreement withthe measurements on noirnals; the curves have maximaat about 500 mgl, and are similar in shape and relativesensitivity. These functions represent the well-knownaction spectrum of the scotopic visual system. However,almost identical findings were obtained for D.M. when,presumably, the dark-adapted fovea was tested. Thisis particularly surprising since the 42' stimulus fieldwould be expected to fall within the rod-free region ofher retina and yield the spectral sensitivity of the pho-topic (cone) elements. By contrast, the maxima of thenormal functions for this stimulus condition are shiftedto about 560 mju and, except for X>650 mzu, there isa considerable decrease in sensitivity as compared withthe peripheral results. But before concluding that rodfunction has been demonstrated in D.M.'s fovea, wemust determine whether the fovea was, in fact, ex-amined. That is to say, can D.M. centrally fixate a dim

"' H. G. Sperling, J. Opt. Soc. Am. 50, 156 (1960).

spot when it is presented against a completely darkbackg>ronldlld ?

The technique of fixation photography under light-and dark-adapted conditions using a modified Zeissfundus camera has been described elsewhere.1 5 Photo-graphs of D.M.'s dark-adapted retina taken while shewas viewing a small dimly illuminated target showedthat she consistently fixates with a para-macular areasituated about 40 nasal to her fovea. Thus, the similaritybetween D.M.'s peripheral and central dark-adaptedcurves results from a fixation anomaly; her "central"dark-adapted curve actually represents threshold meas-urements from a paramacular retinal region. At photopicluminances, however, fixation photography revealed ac-curate foveal fixation, confirming the observations ofFuortes, Gunkel, and Rushton.'

The spectral-sensitivity functions obtained by themethod of increment thresholds are also instructive asregards the nature of D.M.'s visual defect. With aperipheral test field, the achromat's light-adapted (0.55nL) sensitivity curve very nearly parallels her dark-

adapted function. Except for raising the thresholds byabout three log units, the shape of the curve and theposition of the maximum in the region of 500 my arepractically unaltered. For the normal subject (Fig. 3)however, this degree of light adaptation suffices to altersignificantly the form of the sensitivity functions; thecurves are broader, the maxima are displaced to longerwavelengths, and the relative sensitivity in the blue endof the spectrum is enhanced.i" These results suggest thatwhereas light adaptation brings into play photopic ele-ments in a peripheral area of the normal eye, we wereunable to detect photopic activity in a region only 70from D.M.'s fovea. It would obviously be of interest toexamine the effects of higher background luminance, butthe energy available from the monochromator was in-

H

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005

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FIG. 4. Spectral-sensitivity data for subject D.M. Test condi-tions same as in Fig. 3. Also shown are the results for centralmeasurements obtained with a background luminance of 0.055 mL((). Details in text.

16 I. M. Siegel and B. Bruno, Arch. Ophthalmol. 72, 670 (1964).1' R. A. Weale, J. Physiol. 119, 170 (1953).

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May1966 LUMINOSITY FUNCTIONS IN INCOMPLETE ACHROMAT

sufficient to obtain AL values for most of the test wave-lengths when the background was raised to 1 mL.

With a foveal test field (Fig. 4), the increment thresh-old measurements on D.M. clearly exhibit spectral char-acteristics unlike those of the scotopic system; at abackground luminance of 0.55 mL, the curve is moresharply peaked and the maximum is shifted to 560 mu.Although the location of the X.ma is indicative of pho-topic function, there are marked differences betweenthis curve and the corresponding curves for normals.The achromat's sensitivity function is narrower and,on average, about 1.5 log units below that of the normalacross the spectrum. This over-all loss in sensitivity,the subject's poor visual acuity, and the fact that photo-sensitive foveal pigments have not been detected byfundus reflectometry,1 7 suggest that the functioningreceptors in D.M.'s fovea are few in number.

When the background luminance was decreased to0.055 mL (Fig. 4), the spectral sensitivity function be-came bimodal, with peaks at 500 my and 550 mg. How-ever, since we did not attempt to determine our sub-ject's fixation accuracy at this adaptation level, littlecan be said regarding the actual locus of stimulation. Iffixation was intermediate (or wandered) between theeccentric position found in the dark-adapted eye andthe central point used by the light-adapted eye, it ispossible that both foveal and nonfoveal elements havecontributed to this sensitivity function.

Figure 5(A) shows the course of dark adaptationmeasured with a 10 target located 10° below a fixationpoint. Although a relatively high preadapting luminance(2800 mL) was used, the achromat's curve does notshow the early photopic segment seen in the normalfunction; final light thresholds were, however, onlyslightly above the normal's. When dark adaptation wastested with a central 6° stimulus field [Fig. 5(B)], a bi-phasic curve was obtained for D.M.; the "break" be-tween photopic and scotopic segments occurred afterabout 10 min in darkness. However, the photopic por-tion of the curve lies about 1 log unit above the normalfunction.

Results of the dark-adaptation study are consistentwith the previous findings in demonstrating photopicfunction within D.M.'s fovea, but none peripherally. Itis important to note that our subject's fixation difficultydoes not preclude such an interpretation. D.M. fixateseccentrically following complete dark-adaptation, butcentrally at moderate light-adapting luminances. Thus,after extinguishing the 2800-mL pre-adapting field ofthe adaptometer, her eye remained appreciably lightadapted for about 15 min and a relatively bright spotwas required for fixation. We found, by means of fixa-tion photography, that central fixation was maintainedduring this period.

17 W. A. H. Rushton, J. Physiol. 156, 193 (1961).

A10.0

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" 6.0 - -

-J 4.05 ---- --5 0o 15 20 .25 30MINUTES IN DARK

B1 0.0 _.

- 90 L ..480 * c..*..-7.0k *,6.0Fi6.0 '- -

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FIG. 5. Dark-adaptation data for subject D.M. obtained from(A) peripheral and (B) central retinal regions after 7-min lightadaptation to 2800 mL. The dashed lines show the results fornormal subjects.

DISCUSSION

The existence of more than one receptor type in theretina of the incomplete achromat was demonstrated bySloan in her careful analysis of congenital achromatop-sia.3 She noted that although several of her subjects werelike the totally color blind in many respects, they coulddistinguish some colors from greys of the same apparentbrightness. However, the residual color vision was notreadily identifiable with a specific category of colordefect. We experienced a similar situation when testingour subject at illumination levels comparable to thoseused by Sloan. Photopic function was so severely de-pressed that, although D.M. could distinguish high-chroma test papers from grey, extreme wavelength dif-ferences were required for hue discrimination (Fig. 1).In general we can specify that she appears achromaticat illuminances up to 20 ft-c; when the test illuminanceexceeded 37 ft-c (Figs. 1 and 2) it was possible to detecta tritanopic defect in addition to the over-all impairmentof photopic function.

Whether or not a single term, such as "incompleteachromat," or "high-threshold dichromat" may be mostappropriately applied to our subject we shall not say.It would, we think, be awkward to specify differentclasses of visual performance in the same subject bydifferent names at two levels of illuminance. On theother hand, no single precise classification seems to beunequivocally satisfactory.

A recent study of atypical achromatopsia by Black-well and Blackwell4 illustrates further the importance oftesting color discrimination at several luminances. Usinga brightness matching technique, they determinedspectral-sensitivity functions for different luminancesof the standard comparison field. Their data for the"blue monocone monochromats" are particularly rele-vant to the results of the present study. When the centralretina was tested at the lowest luminance level, thesensitivity curve was essentially scotopic in form; ata much higher level, the curve had a maximum at 440mp, indicating activity of a blue-sensitive mechanism.At an intermediate luminance, they obtained a double-humped curve with peaks at 460 mg and 510 mg, whichthey suggested represents the summated response ofrods and the blue-sensitive cones. These results, ob-

SIEGEL, GRAHAM, RIPPS, AND HSIA

tained with the subjects using "their normal fixation,"were considered indications that both rods and blue-sensitive cones are present in the foveae of their subjects.The authors conclude that "probably all cases of con-genital achromatopsia with reduced acuity have bothrod and blue cone receptors."

Our results for D.JM. are in some respects analogousto the experimental findings reported by the Blackwells,but there are notable differences as regards the inter-pretation of the present data. Although D.i. exhibitedscotopic as well as photopic function on tests of 'foveal'sensitivity, the scotopic data cannot be taken as evi-dence for foveal rods. Owing to the subject's eccentricfixation, the actual test locus was probably severaldegrees from the fovea. In addition, the photopic sensi-tivity data do not represent the responses of a blue-sensitive mechanism; on the contrary, D.M1. appears tohave a tritanopic defect at high luminance. Finally, thedouble-peaked function obtained at an intermediateadapting luminance may also be the result of a fixationerror, but we have no objective measurements of fixa-tion to support this view.

Extending the luminance range at which color visiontests are administered may also be of value in the studyof typical (complete) achromatopsia. In many of thesecases a photopic mechanism seems to be functioningat relatively high luminances. Although this mechanismexhibits certain "cone" properties, e.g., a Stiles-Craw-ford effect,"8 a "cone branch" in the dark adaptation, 3" 9

critical fusion frequency, and intensity discriminationfunctions,20 the subjects are totally color blind by routinecolor vision tests. Perhaps the use of more intense chartilluminance would reveal evidence of hue discriminationin some of these subjects.

ACKNOWLEDGMENTS

We wish to thank Professor W. N. Schoenfeld andR. Shlaer for their cooperation during the course ofthis study.

Is M. Alpern, H. F. Falls, and G. B. Lee, Am. J. Ophthalmol.50, 326, part 2 (1960).

19 S. D. Lewis and J. Mandelbaum, Arch. Ophthalmol. 30, 225(1943).

20 S. Hecht, S. Shlaer, E. L. Smith, C. Haig, and J. C. Peskin,J. Gen. Physiol. 31, 459 (1948).

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