JOURNAL OF THE OPTICAL SOCIETY OF AMERICA

Effects of Stimulus Duration upon Spectral Sensitivity of the HumanElectroretinogram

WILLIAM R. BIERSDORF AND ALLEN M. GRANDAWalter Reed A rniy Institute of Research, Washington 12, D. C.

(Received March 20, 1962)

The effects of three stimulus durations on spectral sensitivity of the electroretinogram were examinedunder moderate light adaptation. The durations were 11, 42, and 109 msec. At a low criterion amplitude ofresponse, the 11-msec duration showed lower sensitivity in the green and blue regions of the spectrum thanthe two longer durations. At the red end of the spectrum all curves showed elevated sensitivity of approxi-mately equal amounts. For a moderate criterion amplitude, the curves for the various durations retainedtheir relative positions at the shorter wavelengths. At the red end of the spectrum, sensitivity decreased forall durations, but to a greater amount for the two longer durations. For a high criterion response, the 1 1-msecduration became more sensitive throughout the spectrum; however, it retained a form similar to that forthe tvo longer durations. The curves were presumed to include at least two components: a scotopic processand a red-sensitive process. Possible interpretations of the duration effects on the spectral curves includedthe Bunsen-Roscoe law and the summation of on- and off-responses.

INTRODUCTION

MANY psychophysical experiments have shownM that in the determination of visual thresholds,the energy of the stimulating light flash must be ofa certain constant value. This relation of stimulus lu-minance and duration (IXt=K) is called the Bunsen-Roscoe law or law of Bloch. The law is valid to a limitingcritical duration beyond which thresholds are generallydependent only on the luminance of the light. In ex-periments that have measured critical durations forvarious parts of the retina, it was found that near ab-solute threshold the critical durations were about 100msec, both in the fovea or cone-dominated region," 2

and in the periphery or predominantly rod area.3' 4 Underincreasing light adaptation, however, critical durationswere found to decrease in magnitude to about 20-30msec.9-7 The question arises as to whether this reducedcritical duration is a function of cone activity or otherfactors operating under photopic conditions. Relatedpsychophysical studies are those concerned with the rateof rise of visual sensation with different wavelengths. 8' 9

Analysis of the human electroretinogram has shownthat the Bunsen-Roscoe law is also applicable to themagnitude of the electrical response, with certain quali-fications.l>' 2 The A and X waves prove a closer fit tothe Bunsen-Roscoe relationship than does the B wave.The critical duration for the B wave is not constant, butbecomes shorter for high-response magnitudes. For

I H. W. Karn, J. Gen. Psychol. 114, 360 (1936).2 R. 0. Rouse, J. Opt. Soc. Am. 42, 626 (1952).3 C. H. Graham and R. Margaria, Am. J. Physiol. 113, 299

(1935).H. B. Barlow, J. Physiol. (London) 141, 337 (1958).

6C. H. Graham and E. H. Kemp. J. Gen. Physiol. 21, 635(1938).

6 W. R. Biersdorf, J. Opt. Soc. Am. 45, 920 (1955).R. M. Herrick, J. Comp. and Physiol. Psychol. 49, 437 (1956).M. A. Bills, Psyehol. Motiogr. 28 (No. 127), 1 (1920).

9C. E. Ferree and G. Rand, Am. J. Psychol. 35, 209 (1924).10 E. P. Johnson and N. R. Bartlett, J. Opt. Soc. Am. 46, 167

(1956).11 M. Alpern and J. J. Faris, J. Opt. Soc. Am. 46, 845 (1956).12 W. R. Biersdorf, J. Opt. Soc. Am. 48, 412 (1958).

high-luminance stimuli the magnitude of the B wavedecreases rather than remaining constant for stimulusdurations longer than the critical duration. The B wavecritical duration also becomes shorter under higher lightadaptation.

The X wave of the human electrorktinogram has beenrelated to photopic and especially red sensitivity,"3 -16while the B wave is considered primarily scotopic innature 7 With red-light stimulation, it was found thatthe X wave had a critical duration of about 25 msec at aconstant level of light adaptation, while the B wavecritical duration at low response levels varied from 50-100 msec.12 In order to isolate the dependence of variousreceptor processes upon stimulus duration, it wasthought desirable to extend this analysis to a more com-plete spectral determination for the electroretinogram.The present experiment investigates spectral sensitivityutilizing stimulus durations in the range of previouslydetermined critical durations.

EXPERIMENTAL METHOD

Apparatus

A 900-W dc xenon arc lamp [Hanovia (EngelhardIndustries)] provided the source for the test light stimu-lation. A rectifier power supply operating at 110 V acwas constructed as none was furnished by the manufac-turer. The wiring diagram is illustrated in Fig. 1. Thelamp required 80-90 V dc to start, but after ignitionoperated at 32 V, 28 A dc. A variable autotransformerprovided the necessary range of ac before rectificationby a bridge circuit utilizing silicon elements. A largeamount of filtering was necessary to reduce the ac com-ponents to acceptable levels after rectification. This was

13 K. Motokawva and T. Mita, Tohoku J. Exptl. Med. 42, 114(1942).

'4 E. D. Adrian, J. Physiol. (London) 104, 84 (1945).16 J. C. Armington, J. Opt. Soc. Am. 42, 393 (1952).'1 G. Schubert and H. Bornschein, Ophthalmologia 123, 396

(1952).17 E. P. Johnson, A.M.A. Arch. Ophthalmol. 60, 565 (1958).

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VOLUME 52, NUMBER 12 DECEMBER 1962

SENSITIVITY OF HUMAN ELECTRORETINOGRAM

FIG. 1. Circuit diagram of 900-W dcxenon arc power supply: R-50-A 140-Vsilicon rectifiers, F1 -20-A fuse, P-Powerstat, F2-35-A fuse, L1 -0.006-H40-A choke, B-30-V (five 6-V storagebatteries), L 2-0.001-H 50-A choke,S2 -DPDT pushbutton switch, Ci,C2,-3000 pF, 150-V capacitors, LS-lamp starter, C3-4-AF 600-V capacitor,X-xenon lamp. R1-40 ko.

provided by 7 mH and 6000 ,F of capacitance. To pre-vent damage to the electrolytic capacitors from the highrf voltage used to ignite the lamp, the capacitors weredisconnected by the same pushbutton switch used totrigger the starting circuit. To reduce ac flicker in thelamp further, a 30-V bank of storage batteries was con-nected across the power supply after ignition. The rfair-core transformer in the starting circuit tended tooverheat during prolonged operation of the lamp, so ashorting switch (S4) was closed to bypass the heavyoperating current to the lamp after ignition. It was alsofound necessary to provide forced-draft ventilation inthe lamp housing furnished by the manufacturer to pre-vent lamp failure from overheating.

The ac ripple in the filtered lamp supply was foundto be much greater in current fluctuation than in volt-age. The ripple in the light output of the lamp was alsoproportional to this current fluctuation. The largeamount of filtering used, however, reduced this currentfluctuation to less than 5%; the addition of the batteriesin parallel then further reduced the remaining ripple.

The visual stimulator employed was a two-beam typesimilar to that previously used."8 The test light fromthe xenon arc lamp was gathered by a short-focal-lengthlens and focused on a 2.0-mm aperture only passinglight from the hottest portion of the arc. Immediatelynext to the aperture a rotating sector-disk shutter wasused allowing durations of 11, 42, or 109 msec as cali-brated by a photocell. The onset times for all exposuredurations were equal and less than 3 msec. After di-vergence the beam was collimated and passed througha hand-operated shutter vane to permit single exposures.To protect the eye from infrared radiation, 2 heat filterswere employed. The first was an interference type (FishSchurman No. 6143) which also reflected ultravioletradiation, and the second was an absorbing type (Corn-ing filter No. 3962). The maximum luminance for whitelight measured 89 000 ft-L. The beam then was passedthrough interchangeable Wratten neutral-density filterswhich allowed variation of the luminance in steps of0.3 and 0.4 log unit. Narrow wavelength bands of stimu-lation were provided by passing the beam through in-terchangeable interference filters, G.A.B. type. Acces-

18 W. R. Biersdorf and J. C. Armington, J. Opt. Soc. Am. 47,208 (1957).

sory Corning filters were used with several of the filtersto reduce the energy in the long tails of the transmissionspectra. The bandwidths of the filter combinations at50% of the peak transmittance was 10 to 15 mg andat 10% of the peak was 25 to 50 m/i. The energy calibra-tions for the xenon arc plus filter combinations weredetermined by a Farrand thermocouple and alsochecked with a calibrated RCA type 930 phototube.The transmittances of the neutral density filters atvarious wavelengths were determined by a Caryspectrophotometer.

A tungsten-filament microscope bulb operating at6 V and 2.5 A provided the adaptation field. Both beamswere circular, subtending 520 visual angle, and werepresented superimposed to the subject in Maxwellianview. Crosshairs in the adaptation beam enabled thesubject to maintain central fixation. The diameter ofboth beams at the subject's pupil was 2.0 mm. The sub-ject's head was kept aligned with the stimulator bymeans of a biting board coated with dental-impressionwax. The adaptation field was maintained at a lumi-nance of 2.8 ft-L.

1420 .,, ' 1, i'2f X.. -....

120 2.0 49o 3 23 212 /

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FIG. 2. Amplitude-luminance curves for 6 of the 12 test wave-lengths. Abscissa shows neutral filtering down from highest avail-able luminance. Luminances for different wavelengths are not ofequal value. Ordinate displays amplitude of the response in !uV.Subject MH.

1403December 1962

Is

I10. VA

AND A. M. GRANDA

Electroretinograms were recorded with a contact-lenselectrode,"9 and a reference electrode on the forehead.The electrical responses were amplified by a direct-coupled amplifier and displayed on a dual-beam oscillo-scope, one beam of which recorded a stimulus timemarker. Photographs of the oscilloscope tracings weretaken with a Grass Kymograph camera. The responseswere simultaneously recorded on a Grass model III Delectroencephalograph.

Procedure

Before an experimental run, each subject was lightadapted for 10 min by exposure to the adaptation field.A test flash, superimposed on this field, was then pre-sented at regular intervals throughout the run. Eachflash represented a particular combination of duration(11, 42, or 109 msec), wavelength (peaks at 423, 445,469, 493, 515, 532, 555, 571, 600, 607, 627, and 640 mr,)and luminance (neutral density filters ranging over 4log units). Intervals of 2 minutes between flashes wereused for luminances corresponding to densities from0.0 down to - 1.6 log units, thereafter for flashes of de-creasing luminance one-minute intervals proved suffici-ent to allow recovery from the previous flash. A normalexperimental session consisted of 70 to 80 flashes withappropriate periods of rest to insure the subject's easeand comfort. Three subjects were used in the presentset of experiments.

RESULTS

Responses were measured from the most negative por-tion of the A wave to the most positive portion of theB wave. The implicit times (latencies to peaks) of theERG's were in the range 40-60 msec for the high-luminance responses regardless of wavelength or stimu-lus duration. Implicit times became longer for lowerluminance levels and reached 100 msec in some cases.Double-peaked responses sometimes appeared for themiddle-wavelength stimuli, and in addition the longerstimulus durations tended to produce longer implicittimes.'2 Only total positive height was measured as datawere available over a longer luminance range than fordouble-peaked positive responses or A waves.

A display of luminance-amplitude curves for 6 of the12 test wavelengths used in the present experiment areshown in Fig. 2 for subject MIH. The curves show ageneral rise to a short plateau and then a further risein response to brighter flashes of light. As may be seen,the plateau is most evident at the shorter wavelengthsand also better defined for the longer durations of 42msec and 109 msec. It may be noted that the 11-msecflashes generally reach higher amplitudes at most wave-lengths than the corresponding durations of 42 msec and109 msec.

It is also evident that differences in sensitivity arepresent that accrue from the different durations. For

19 L. A. Riggs, Proc. Soc. Exptl. Biol. Med. 48, 204 (1941).

low-response magnitudes at the blue end of the spec-trum, the 11-msec durations are less sensitive thanthose of 42 or 109 msec. That is to say, for a given heightor response, a brighter flash at 11 msec must be used tomatch in height those of the longer durations. In theregion of 555-571 m,4, this sensitivity of the 11-msecflashes shifts relative to 42 and 109 msec resulting in anincreasing sensitivity toward the red end of the spec-trum. This increased long-wavelength sensitivity of theshort duration is most evident at 600 and 607 mu.w

For subjects DWK and JK the changeover in sensi-tivity of the 11-msec flash follows the form displayedin Fig. 2. The changeover begins at 515 m/u for subjectJK, and at 571 for subject DWK. For all subjects the11-msec stimuli produce lower sensitivity at the blue

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FIG. 3. Spectral sensitivity for subject MH. Relative luminancerequired to produce a 20-,uV criterion response at each testwavelength.

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11 MSEC

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FIG. 4. Spectral sensitivity for subject MH. Relative luminancerequired to produce a 60-,uV criterion response at each testwavelength.

1404 W. R. BIERSDORF Vlol. 52

I

SENSITIVITY OF HUMAN ELECTRORETINOGRAM 1405

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FIG. 5. Spectral sensitivity for subject MH. Rrequired to produce a 120-,uV criterion respowavelength.

end of the spectrum and higher sensitiend.

The spectral sensitivity curves weretermining the amount of luminance reduce a constant height of response anddetermination with the stimulus-energythat wavelength. Where the criterion heiluminance curve more than once, allaveraged. Curves of all stimulus durationin Figs. 3-5 for subject MH. Althoughtivity is not measured, curves in all figu:proper ordinate positions relative to ealow criterion height of 20 pV (Fig. 3stimuli produce a curve with low sensiti-end of the spectrum; the 42- and 109-mshigh sensitivity with little difference betthe red end of the spectrum, all duratvated sensitivity and the curves thatapproximately equal heights.

For a medium criterion-response he(Fig. 4), the relative positions of the curend of the spectrum are similar to the IThe 11-msec sensitivity is lower than theequal heights of the 42- and 109-msec sthe red end, relative sensitivities for allcreased, the 11-msec duration remainitive than the two longer durations.

For a high response criterion of 120 juvariability of the curves increases. Icriterion level was chosen so as to attemithe noticeable plateau level in the lumin;curves. The curves so obtained show hi'for the 11-msec duration than for the lobut the relative shapes of the sensiti-,similar. The higher red sensitivity of thc

tion seen in the previous figure is no longer apparent.Subject DWK showed spectral curves similar to theones illustrated for subject MH. Subject JK, however,showed higher sensitivity near 550 m~s rather than at600 mrn for the 11-msec duration at medium responseheights.

DISCUSSION

The amplitude-luminance curves found in this ex-periment agree with those of previous experiments, 1 2 0

in showing a plateau at high luminance levels followedby a secondary rise at even higher luminances. In agree-ment with previous results, this plateau was more pro-nounced at the longer durations than at the short dura-tion. In this experiment, the plateaus were more evi-dent for short and medium wavelength test flashes than

* 700OO for long wavelengths. This is consistent with a previousexperiment where no plateau was found for red test

elative lumin flashes measuring X-wave height alone.12 The questionnse at each test is therefore suggested whether this plateau constitutes

a sort of "rod-cone break" analogous to the break foundin psychophysical experiments. The obtained spectral

vitv at the red curves provided a partial answer to this. At a low-criterion height (Fig. 3), the most sensitive portion of

derived by de- the spectral curves was similar to the standard CIEquired to pro- scotopic-sensitivity curve. In addition there was acombining this shoulder representing high red sensitivity.15 A highercalibration at criterion, on the other hand, reduced the magnitude of

ght crossed the the red process, as has been found previously.1 8 Thecrossings were ERG spectral curves were also more sensitive than thes are presented CIE scotopic curve in the blue region (shorter than 500absolute sensi- my) of the spectrum.2 A major sensitivity componentres are at their at high-response levels was still scotopic, however, inso-ch other. At a far as could be judged from the present data. Thus the) the 11-msec plateau, while possibly reflecting the presence of coneTity at the blue processes, did not necessarily represent the elimination-c stimuli show of rod activity. The high response-criterion curvesween them. At showed greater variability due to the criterion fallingions show ele- at the level of the plateau where multiple values wereresult are at obtained for some test wavelengths and not for others.

This was the case for the high 445-mg sensitivity at theight of 60 uV 42-msec duration. The spectral sensitivities at high-ves at the blue response levels, however, seemed to be similar for all)revious figure. stimulus durations. Even though the short-durationapproximately luminance curves extended to higher amplitudes thanensitivities. At the longer durations, this apparently did not produceI durations de- marked relative differences in spectral sensitivity.ig more sensi- The effects of stimulus duration on low-response mag-

nitudes were clearly color dependent. In the scotopicV (Fig. 5), the region of the spectrum both the amplitude-luminanceThis particular and the spectral curves showed differences which couldipt to be above be interpreted on the basis of the Bunsen-Roscoe law.sance-amplitude In this region, the 11-msec durations produced smaller,Yher sensitivity responses for equal luminances than did the longernger durations, H. Bornschein and R. D. Gunkel, Am. J. Ophthalmol. 42, 239

rity curves are (Part II) (1956).11-msec dura- 21 J C. Armington, J. Opt. Soc. Am. 49. 1169 (1959).

December 1962 1405

W. R. BIERSDORF AND A. M. GRANDA

durations. There was not much difference between themagnitudes of the two longer-duration responses. Thiswas true both for low- and medium-criterion responseheights. The results under these conditions may be in-terpreted to mean that the critical duration for theapplicability of the Bunsen-Roscoe law in the scotopicspectral region was in the neighborhood of 40 msec.Previous experiments have found the critical durationfor the B wave under more dark-adapted conditions tobe near 100 msec.'0 1

2

In the red region of the spectrum (near 600 mu), how-ever, the Bunsen-Roscoe interpretation is not adequate.The law would predict lower response sensitivity forstimulus durations shorter than the critical duration.The response sensitivity for the 11-msec stimuli, how-ever, exceeded that of the longer durations for themedium-response criterion. The region of this enhancedsensitivity for short-duration stimuli corresponded withthat of a hypothesized red-sensitive process describedin several previous experiments.' 18'21

One possible interpretation of this short-durationlong-wavelength enhancement involves the summationof on and off responses. It has been shown that the off

effect is larger for shorter-flash durations. 22 The offeffect has also been supposed to be cone dominated,23 24

although direct determinations are difficult because ofits very small magnitude. The sensitivity measures ofthe present experiment were determined by the ampli-tude at the most positive point which occurred 40-60msec after the light-flash onset for the medium-criterionspectral curves. It is possible, therefore, that the 11-msecflashes revealed the summated sensitivity of on and offresponses while the longer durations reflected primarilyon-response sensitivity. For the low-criterion spectralcurves, presumably the magnitude of the off effect wasnegligible. Another possibility to be considered in in-terpretation would be an interaction of stimulus dura-tion and stray light affecting the nonfocal retinal areas.

ACKNOWLEDGMENTS

The authors wish to gratefully acknowledge theassistance of John Kimbrough, Kent Clements, andHarold Lawson.

22 W. Best and K. Bohnen, Arch. Ophthalmol. Graefe's 158,568 (1957).

2a J. Heck, Acta Physiol. Scand. 40, 113 (1957).24 C. I. Howarth, J. Opt. Soc. Am. 51, 345 (1961).

1406 Vol. 52