Frequency dependence in scotopic flicker sensitivity

0042.6989!8553.00+ 0.00 Copyright E 1985Pergamon Press Ltd

vicion Res. Vol. 25. No. I. pp. ll5-127. 1985 Printed in Great Britain. All rights rcse~ed

FREQUENCY DEPENDENCE IN SCOTOPIC FLICKER SENSITIVITY * R. W.

NYGAARDt$

and T. E. FRUMKES

Department of Psychology, Queens College of CUNY, Flushing, NY 11367, U.S.A. (Received 23 September

1983; in revised form 12 June 1984)

Abstract-Sensitivity to rod-mediated (scotopic) flicker was parametrically studied in the parafoveal retina of human observers. Confirming prior studies, the present results show that sensitivity to scotopic flicker has many similarities to that at photopic levels. Specifically, our results show that the frequency response function for scotopic flicker is characterized by both low- and high-frequency cutoffs and that sensitivity to low frequencies is described by Weber’s law. Overall, however, scotopic flicker sensitivity is characterized by higher increment thresholds and lower frequency tuning than photopic flicker. The influences of spatial factors and the prevailing level of illuminance on sensitivity is sufficiently different for relatively low (< 3 Hz) and relatively high (> 5 Hz) temporal frequencies to suggest that they may be mediated by different channels. This possibility is also suggested by selective adaptation experiments. These show that adaptation to flicker frequencies of 3, 5, and 7 Hz have a similar influence on sensitivity to subsequent flicker which is different from the influence on I Hz flicker adaptation. Results are compared with prior evidence for channeling within both the scotopic and photopic visual systems. Scotopic flicker

Rods

Adaptation

Temporal channels

The work of Ives (1922a) first established

that the temporal frequency response of the human observer can be described as a bandpass filter. Subsequent investigations, in which the depth of modulation of a flickering stimulus was adjusted for threshold, have indicated characteristic differences in the factors which limit sensitivity to lower and higher frequencies. For example, Kelly (1961a) studied sensitivity to sine wave flicker at different levels of d.c. (or time-averaged) illuminance, including one scotopic (rod-mediated) and many photopic (cone-mediated) levels. His photopic data showed the following. For frequencies approaching the high frequency cutoff, the a.c. (or sine wave amplitude) component of flicker necessary for threshold detection was independent of the d.c. itluminance, an observation in line with the operation of a linear system. For low frequencies, however, the ratio of a.c.-d.c. illuminances seemed to determine threshold sensitivity as would be predicted *Supported in part by NIH grant EY01802 awarded to T. E. Frumkes and EY03674 awarded to J. M. Enoch. tPresent address: School of Optometry, University of California, Berkeley, CA 94720, U.S.A. IThis article is based on work presented in partial fulfillment of the Ph.D. degree in Neuropsychology. City University of New York. flhroughout the text, the terms “compressive” and “compression” are used in a manner consistent with systems analysis and refer to a particular non-linear relationship between output and input. According to this usage, any attenuation of sensitivity with increasing input (e.g. Weber’s law or the squareroot relationship) is “cornpressive”. In fact, the physiologicuf changes in photoreceptors which are largely responsible for Weber’s law have been interpreted as reflecting both a change in setpoint (“cellular adaptation”) and “response compression” (Normann and Perlman, 1979).

LEDs

by the Weber-Fechner relationship. Intermediate frequencies demonstrated illuminance non-lineatities less compressive$ to sensitivity. Earlier theorists attempted to explain the observed differences in high and low frequency flicker in terms of the operation of a single channel with several different series stages (e.g. Ives, 1922b; delange, 1961; Kelly, 1961b, 1969b; Fuortes and Hodgkin, 1964, Roufs, 1972b). However, the differences underlying high and low frequency flicker perception are great enough to suggest that different channels may mediate flicker sensitivity as has been suggested by several more recent investigators (Smith, 1971, 1973; Tyler, 1975; Conner and MacLeod, 1977; Conner, 1982). To test this possibility, frequency adaptation experiments have been performed at photopic illuminance levels with the goal of selectively adapting out (reducing the sensitivity of) a temporal frequency process and have yielded generally positive results (Pantle, 1971; Smith, 1971; Nilsson et al., 1975). But, the results present interpretive difficulties since photepically adapted human vision is mediated by three types of photoreceptors, each of which is likely to have unique time constants (e.g. see Wyszecki and Stiles, 1982) and different frequency-response functions (Kelly, 1962). For this reason, it is difficult to ascertain whether isolated “temporal” channels mediating photopic flicker merely reflect differences in the maximally responsive set of photoreceptors. The present study was initiated with the goal of determining whether one or more postreceptor neural channels mediate flicker sensitivity. In order to avoid the confounding influence of several types of photoreceptors, conditions were restricted to situations in which only one type of photoreceptor, the rods, were I15

R. W.

1.16

NYGAARD

mediating vision (e.g. parafoveal stimulation with low levels of illuminance). The existing mesopic and scotopic flicker literature suggests several similarities with photopic flicker. For example, small-field mesopit flicker sensitivity measured without a surround can be described as a band-pass function if measured down to frequencies well below 1 Hz (Ives, 1927a), Indeed, under these conditions, the scotopic Bicker response differs oniy in its dynamic frequency range and frequency of maximum sensitivity, both of which are less than at photopic levels (Roufs, 1972a). Furthermore, under constant levels of mesopic or scotopic light adaptation, the first harmonic predicts at least the high frequency response both psychophysically (Ives, 1922a) and electrophysiologically in rod achromats (Gouras and Gunkel, 1964), again as is the case for photopic flicker (deLange, 1954, 1958a, 1961). Finally, under changing conditions of light adaptation, electrophysiological data in rod achromats appear to suggest a (nonlinear) compression of temporal modulation sensitivity (Gouras and Gunkel, 1964), a phenomenon similarly found at photopic light levels for frequencies under 15 Hz (Kelly, 196la). This has been confirmed psychophysically in normals for illuminance levels under 1 Scot. td and for frequencies between about I-15 Hz (Smith, 1973; Conner, 1978, 1982), and in a rod achromat at high illuminance levels for frequencies between I and 14 Hz (Skottun et al., 1980). These last investigators could only find evidence of a linear rod response by employing higher levels of illumination and higher frequencies. Such data cannot be obtained in the normal observer without using special isolation techniques (e.g. see Conner and MacLeod, 1977) because of the much greater sensitivity of cones. Since previous data have not fulty characterized the properties of rod vision in the normal observer, the present study of scotopic flicker within the parafovea1 retina consists of two different parts. In part 1, we parametrically studied the influence of d.c. illuminance and spatial variables on flicker sensitivity. These results suggest that for frequencies under 15 Hz, rod and cone-mediated flicker sensitivity differ mainly in that rods have a much longer integration time (i.e. a band-pass peak at lower frequencies) for luminous flux. In Part 2, we attempted to determine whether one or several parallel channels mediate rod vision in the temporal frequency domain by means of selective frequency adaptation experiments. These results suggest that scotopic flicker may be mediated by several parallel channels. Some of this work has been presented in abbreviated form elsewhere (Nygaard and Frumkes, 1978; Goldberg er al., 1982; Goldberg et al., 1983). METHODS AND MATERIALS

Oplical stimulator

All stimuli were presented to the observer’s right eye by means of a 4-channel optical system with

and T. E. FRLMKES

u NP Fig. 1. Schematic of the four-channel ~~axwei~ian view or&al system used t~ro~out the study. Sl was a tungsten source whose spectral output was de&mined by an interference filter olaced at F. Other elements include LED

sources St-sd, beamsplitters BI-B3, and neutral density absorption

wedges WI and W2. NP corresponds nodal point of the observer’s right eye.

to the

separate sources for each channel as indicated in Fig. 1. Source Sl was a 6 V 18 A tungsten lamp (GE CPR projection lamp) which provided either a 30 deg field (for light adaptation purposes) or an annulus of 2.5” inner, 6.5” outer diameter and was used for calibration purposes. The waveIe~gth of this fietd was fixed by interference filters placed in filter rack F; the spatial position and configuration of this field could be altered by changing the position and type of aperture placed at micromanipulator A 1. A 4 log unit neutral density wedge (Wl) as well as additional fixed neutral density filters placed at F controlled the illuminance of this field. The other three sources were General Instrument LEDs which, depending on the demands of a particular experiment, were either “red” or “green” (respectively, models MV 5152 and MV 5252). The red LED source 53 provided a central fixation target, while the other two sources (red and green) presented either steady or fiickering stimuli. The depth of modulation of all flickering stimuli was determined according to the circuit of Nygaard and Frumkes (1982b, Fig. 2), which over the depth of modulations employed throughout this study (O-70%) provided almost perfect linear control. The average illuminancc level of Aickering stimuli was determined by adjustment of either wedge WI or W2. The illuminance of all stimuli from LED sources was controlled by varying wedge WI or W2. A series of prisms and beamsplitters presented all visual fields in MaxweIlian view to the observer’s right eye. The final

Scotopic Bicker sensitivity source image was about 2 mm in diameter, considerably less than the size of the natural pupil in this study of rod vision. The illuminance of all stimuli was directly calibrated with an EC&G radiometer according to the technique of Nygaard and Frumkes (1982a), and checked according to a matching procedure (Frumkes and Sturr, 1968). Photopic illuminance of LED elicited stimuli was also checked by matching them in brightness to the white light stimuli. Calibration of scotopic iliuminance was achieved by matching absolute threshold of colored and white light stimuli. The waveforms of all LED sources were continuously monitored on an oscilloscope according to the technique of Nygaard and Frumkes (1982b). All data presented below were collected according to the psychophysical method of adjustment. A number of precautions were observed in collecting the data in Figs 3-l 1 since continually exposed stimuli in the parafoveal retina are particularly susceptible to both Troxler fading and flicker-related adaptation (see Part 2 of our experiment). Prior to data collection, the modulation depth of the flickering test stimulus was always set at a pseudorandom value known to be subthreshold; in making his judgment, the observer was instructed to keep the modulation depth close to threshold and the final threshold adjustment was always “ascending”. Modulation threshold had to be obtained within a 30 set interval, and after obtaining it, there was a rest period of at least 90 set before further data collection. Furthermore, to observe the test stimulus, the observer was required to switch a normally steady field to a flickering one of the same d.c. illuminance by depressing a momentary pushbutton. In the case of selective adaptation by above-threshold flicker of a specified frequency (Part 2), adapting stimulus presentation and withdrawal were “windowed” by the subject slowly opening and closing his eyes at the initiation and termination (respectively) of an adapting interval. While this procedure is noisier than, e.g. the use of a Gaussian temporal envelope, abrupt transitions are nevertheless reduced. Whenever suitable, all data were presented to a subject within a session in which stimulus sequence was randomized; after a break, the counterbalanced sequence was presented. Unless indicated otherwise, every datum presented below represents means from at least 4 such experimental sessions. THE ROD SPECIFIC NATURE OF GREEN LED STIIMULI

Throughout this study, we wished to ascertain that rods alone were responding to the flicker elicited by green LED-derived stimuli. We decided against the use of traditional rod-isolation techniques (Aguilar and Stiles, 1954) since large background fields have recently been reported to produce unwanted rod-cone interactions (Buck and Makous, 1981). Rather, we

117

deemed it wiser to keep stimuli at iliuminance levels that were below cone threshold as estimated from several control experiments. In the first of these, sensitivity to the green stimulus was continually assessed following adaptation to a 50,000 td. white light for 30sec. The lowest function in Fig. 2(a) represents the threshold of a 500 msec duration flash (presented once every 2 set) and the resulting coneplateau (at -0.8 log Scot. td) indicates an extreme estimate of cone sensitivity. This value is lower than the peak (a.c. + d.c.) illuminance value represented in Figs 5-11 (indicated by the dashed line). With the exception of data obtained with a d.c. illuminance of -0.7 and -0.4 log Scot. td, this is also lower than the corresponding peak illuminance values plotted in Figs 3 and 4. Much less restricted (though more reasonable) estimates of cone flicker sensitivity are indicated by the other control data of Fig. 2. For all these remaining data, a sinusoidally flickering stimulus was continuously presented at a modulation depth of 70%. In one group of experiments, the observer adjusted the illuminance of a continuous sinusoidally flickering stimulus of fixed frequency throughout the time course of dark adaptation so that flicker could just be perceived. These data are represented by the large symbols in Fig. 2(a), and the ordinate expresses the peak illuminance of a flickering stimulus (not the d.c. illuminance as in all subsequent figures) at the indicated flicker frequency. The anomalous rise in threshold obtained with 8 and 9 Hz flickering stimuli involves a type of rod-cone interaction described in a separate communication (Goldberg et al., 1983). For the data represented by Fig. 2(b), the observer varied the frequency as a function of stimulus illuminance. The plot is very similar to traditional plots used to derive the Ferry-Porter relationship (e.g. see Hecht and Schlaer, 1936). Disregarding the rod-cone interaction of Fig. 2(a) (which is not apparent after 25-30min in the dark), the data for 1 Hz and above possess cone plateaus at light levels at least 0.3 or 0.4 log units above those examined in the flicker stimuli of corresponding frequency in all the experiments which follow and about a log unit above those in the critical experiments illustrated by Figs 5-l 1. In Fig. 2(b), the lowest frequency down to which the Ferry-Porter relationship is seen to extend is 11 Hz. Therefore, with the possible exception of the 11 Hz data (in Figs 3 and 4), our control plots show that all our data in Figs 3-l 1 involve illuminance values for which cones are insensitive to flicker. Finally, Goldberg and Frumkes (in preparation) have since replicated all the data in Figs 2 and 3 using flickering stimuli generated by a green LED, a red LED, and a red and green LED operated in counterphase. For the latter situation, red and green stimuli were equated for modulation depth and scotopic d.c. illuminance; but the red LED had a 1.6 log unit greater photopic intensity so that cones alone were

R. W.

NYGAARD

and I-. E. FRLWKLS

I 30

/ 20 Time

Pwk

(b)

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30 t

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( min 1

in dark

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Fig. 2. The influence of adaptation on sensitivity to 2” green flicker. In (a), the stimulus illuminance necessary for pulse and flicker detection is plotted during the time-course of dark adaptation. Data were obtained with either a SOOmsec pulse (small squares) or with 70% modulated sinusoidat flicker of the indicated frequency. In (b), critical gicker frequency for sinusoidal Aicker of 70% moduiation depth is plotted as a function of the illuminance of flicker. For both coordinates, in order to clarify the range over which the green LED (predominant wavelength of 565 nm) primarily stimulates rods, all plotted values specify Peak (a.c. + dx.) Itluminance. For both sets of coordinates, the dashed lines indicate the illuminance of the test stimulus used throughout the experiments described by Figs 5-I I. See text for

further details. presented with flicker. Comparison of these three types of data show that under the present range of ilIuminance levels, cone sensitivity to flicker is insufiicient to significantly influence modulation thresholds. STlMULUS PARAMETERS AlW OBSERVERS

All data were collected with a test stimulus consisting of a green flickering disc presented 7 deg from fixation in the temporal field of the right eye. With the exception of Fig. 6 (in which case the stimulus

diameter was varied), this test stimulus was 2 deg in diameter. With the exception of the experiment portrayed by Fig. 5, data were collected when the flickering test stimulus (and the fixation target) was presented alone. In the case of Fig. 5, a concentric red or green annulus (LED generated) of 2.5deg inner and 6.5 deg outer diameter surrounded the 2deg flickering test stimulus. Two observers were used throughout thlq study. P.C. was a 25-yr-old emmetropic male. R.N., the first author and aged 3 1 years, wore corrective spectacles throughout ex~~mentation. In some cases data were

119

Scotopic flicker sensitivity

collected for several additional observers. Unless there were reasons to suspect systematic differences between observers, data are presented only from the observer studied most thoroughly. Prior to data collection, the observer always dark adapted for 30 min and then aligned himself with the optical system with the aid of either 2 chin-and-head rest or a full-mouth bite bar. PART

I: PARAIMETRIC

STUDY

OF ROD FLICKER

Procedure One of the following three procedures were used in collecting all data in Part 1. (A) Determination of the injuence of d.c. illuminance and frequency on scotopic flicker sensitivity.

In a given experimental session, all stimuli were presented at one d.c. level of illuminance. The observer was presented with a Pickering stimulus of subthreshold modulation and then adjusted its modulation depth so that flicker could just be determined. After a second threshold was so obtained, flicker frequency was changed and the procedure was repeated. In the course of an experimental session, about 12 frequencies were presented in a randomized order; after taking a 10 min break, the same frequencies were presented in a counterbalanced order. All data in Figs 3 and 4 were obtained in two such experimental sessions. (B) Influence of surround iihtmirtance on low (1 Hz) and high (7 Hz) frequency rod fficker. In a given

experimental session, red and green annuli (generated by LED sources) with illuminances of either -2.0, -0.8, and -0.2 or - 1.7, - 1.1, -0.5, and -1.4, 0.1 log Scot. td were presented with annular illuminance and hue and flicker frequency (1 or 7 Hz) randomized. The d.c. illuminance of fficker was fixed at - 1.3 log scat. td. Otherwise, the same procedure was followed in each experimental session as in (A), above. (C) Influence of stimulus size and frequency on flicker sensitivity. The same procedure was used as in (A), above except that the same d.c. illuminance Ieve (- 1.3 log scat. td) was used throughout and only 7 stimulus frequencies were studied. In any given experimental session, data were only collected with two of the three sizes of stimuli employed. All 6 permutations of stimulus size (taken two at a time) were presented in this experiment. Results Injuence of average iliuminance and frequency on scotopicflicker sensitivity. For observer P.C., Fig. 3

shows on logarithmic coordinates, the modulation sensitivity as a function of flicker frequency for 5 different levels of d.c. illuminance. Foffowing the convention of Ives (1922a) and later workers in this and all other plots, an increase in sensitivity is indicated by an upward shift on the ordinate. Hence in this figure, the modulation amplitude (i.e. the a.c.

I

I

I

I

I,

0.6

1

2

3

45

,,,

7

9

11

Frequency (Hz 1 Fig. 3. Scotopic frequency response functions for observer p.C. and obtained with 5 different d.c. illuminance values (indicated to the right of each function in log smt. W. AS indicated in the text, the threshold a.c. iiiuminance is shown on the ordinate as a function of flicker frequency. In this and all subsequent figures, an increase in threshold is represented by a lowering of the ordinate position.

itluminance in log Scot. td) is plotted such that higher ordinate positions indicate lower thresholds. Figure 3 shows two similarities with analogous foveaf data obtained with photopic stimuli (e.g. the 1deg disc with dark background of Roufs, 1972a, Fig. 3). That is, as the d.c. illuminance level increases, overall flicker sensitivity tends to increase. In addition, all d-c. iiIuminance levels produce functions with evidence of both a low and high frequency falloff. Two differences are also apparent. First, the scotopic system is tuned to much lower frequencies with peak sensitivity between 2 and 3 Hz (vs 10-20 Hz at photepic levels). Secondly, at photopic levels frequencies near the CFF of each function describe a common envelope, a finding consistent with the operation of a linear system. This is not the case for the scotopic data plotted in Fig. 3. Further analysis of such data is better made by a derived plot such as Fig. 4 which shows data from both observers (on separate coordinates). In this plot, retative moduIation sensitivity is indicated on the ordinate as a function of the log of the time averaged illuminance level on the abscissa for several different flicker frequencies. In such a plot, We&r’s law is indicated by a function with a slope of zero, the operation of a linear-like system with a slope of i, while a devries-Rose (squareroot) refationship is represented by a slope of I/2. As is the case for photopic flicker (Kelly, 196la), al1 functions obtained with relatively lower frequencies (in the present case, for frequencies between 0.6 and about 4 Hz) describe

R. W. SLGAARDand T. E. FRCMKES

40

50

’1 _____-&____e-.._ __‘_____~~___~______________.___

j

Fig. 4. Incremental sensitivity to scotopic flicker for two observers. The data for observer PC. (upper coordinates) were derived from Fig. 3; similar data were used to obtain the results for observer R.N. (lower coordinates). In both cases, threshold modulation (a.c./d.c. ratio) is scaled logarithmically on the ordinate against d.c. illuminance for the indicated flicker frequencies. In all cases, the error bars on the right indicate f 2 SE for the adjacent datum having the largest variability. The labeled dashed functions indicate the slopes of a linear function and a function adhering to Weber’s law. a common horizontal line. This indicates a Webers law relationship with Weber fraction of about 0.15 for both observers. Data obtained with higher frequencies and illuminance levels over - 1.1 log scat. td also tend to have a slope of 0, but describe different Weber constants. At dimmer illuminance levels, however, these data show a different tendency which may describe a family of straight lines with slopes between about 0.2 and 0.6. On the other hand, there is variability in these data which could also suggest a transition from a devries-Rose to a Weber compression relationship (see Smith, 1973). Injuence of spatial manipulation on scotopicjlicker sensitivity. There are well known, frequency-specific spatial influences on photopic flicker sensitivity. For example, the parametric data obtained by Kelly (1961a) with a flickering ganzfeld show relatively greater sensitivity to higher frequencies and relatively less sensitivity to lower frequencies than those obtained with smaller, sharply focused flickering gelds and dark surrounds (Kelty, 1959; Roufs, 1972a). Furthermore, with such a small flickering test stimulus, there is evidence that a steady annular surround tends to increasingly improve sensitivity as frequency is lowered (Roufs, 1972a). Comparable scotopic data are presented in Figs 5 and 6. In one experiment, we assessed the influence

j

Fig. 5. The influence of a 2’ wide annular surround (illuminance indicated on the abscissa in log Scot td) on modulation sensitivity to a 2’;diameter flickering stimulus of - 1.3 log scat. td and for observer R.N. Data were obtained with both a I Hz (upper set of functions plotted as triangles) and 7 Hz (lower set of data plotted as circles) test stimulus, and when the annulus was provided by either a red (sohd symbols) or green (open symbols) LED. The horizontal dashed lines indicate modulation thresholds obtained in the absence of an annulus k2 SE. The vertical dashed line labeled “B” is the d.c. illuminance of the test stimulus,

of an annular surround of 2.5 deg inner and 6.5 deg outer diameter on sensitivity to I and 7 Hz flicker. (Since the test stimulus was 2 deg in diameter, this stimulus configuration resulted in a 15’ wide dark “ring” between the disc and annulus.) The annulus had a predominant wavelength at either 560 or 635nm to assess the possible influence of cones on rod flicker sensitivity. In Fig. 5, modulation sensitivity is plotted as a function of annular illuminance for observer R.N. Since the abscissa is expressed in

Scot. td, the red and green annuli were equated for rods while the red annulus had a much greater influence on cones (for further rationale, see Barris and Frumkes, 1978). Notice that regardless of annular wavelength and test flicker frequency, sensitivity at first increases, then decreases with increase in annular illuminance. Possibly due to the lack of continuity between annulus and test disc, peak flicker sensitivity was obtained with a stimulus about 0.5 log units brighter than the test disc. This is consonant with earlier photopic findings (Berger, 1954). Also, except for the most intense annulus (which coukl also involve a cone influence), there is no evidence for a differential annular influence on I vs 7 Hz flicker. This also agrees with earlier photopic findings (Wisowaty, 1979). Regardless of the underlying mechanism, the annular influence cannot be accounted for by stray light alone. Recall that Fig. 4 shows that for both 1 and 7 Hz Aicker, sensitivity to flicker of the test disc is described by a compressive relationship. Thus, a stray light argument would predict that increasing annular illuminance should monotonically decrease flicker sensitivity, a finding at odds with the observed inverted U-shaped functions.

Scotopic flicker sensitivity

121

vision mainly in its low temporal tuning characteristics. In other respects, our data show that rod-29 mediated flicker sensitivity is quite comparable to that of cones. -27; P First, cone-mediated responses to flicker undergo a -2.5 3 gradual linear to Weber law compression of sensi1: tivity with increasing intensity. This successive com-23 g pression begins at low frequencies and proceeds to .E higher ones as intensity is raised (Kelly, 1961a; Roufs, 1972a). Our rod responses are similar except that some compression is always evident even at relatively high frequencies (e.g. 9 Hz). This agrees with previously reported findings (Smith, 1973). Linear-like behavior in scotopic increment thresholds is approached but never reached at levels over 1 td (ConFig. 6. Influence of test stimulus size (as indicated by the ner, 1978). different shaped symbols) on sensitivity to flicker of different Second, in the presence of an annular surround of frequencies (indicated along the ordinate). For all three sets equal illuminance, the response at photopic light of data, the left ordinate indicates the threshold modulation levels is better to frequencies under 10 Hz than to (a.c./d.c. ratio) for the - 1.3 log scat. td flickering test stimulus. The dashed function and right ordinate indicate those over 10 Hz (Kelly, 1959; Roufs, 1972a). In our the relative sensitivity increase resulting from an increase in experiment, relatively iow (1 Hz) and high (7 I-It) the flickering stimulus diameter from 314“to 8”. See text for rod-sensitive frequencies are processed similarly by further explanation. rods in the presence of a luminous surround except at very high surround intensity levels. Even at these levels, it is possible that light scattering from the Figure 6 shows the sensitivity to flickering stimuli of 3/4, 2, and 8 deg diameter (along the ordinate) as annular surround serves to significantly reduce modulation depth in the spatial locus of flicker and to a function of flicker frequency for observer R.N. For result in the high intensity behavior we observe.* clarity, +2 SE of the mean error bars were not Both 1 and 7 Hz frequency sensitivities are well included but were generally equal to twice the dimenwithin the range of cone-mediated flicker that are sions of the plotted symbols. Regardless of frequency, facilitated by the presence of a steady annular sursensitivity to flicker increases as stimulus diameter increases. In order to examine the possibility of round (Kelly, 1959; Keesey, 1970; Roufs, 1972a). Therefore, our rod-mediated annular results again frequency specificity, we constructed several derived characterize rod-mediated flicker sensitivity as complots. For example, the dashed function and right ordinate display the relative sensitivity to flicker for parable to cone-mediated processing. Third, with changes in area there is evidence of 8 vs 3f4deg fields. Notice that as flicker frequency modest frequency dependent differences in area inteincreases up to about 2 Hz, the relative sensitivity gration of flicker sensitivity on either side of 2 Hz. monotonically increases and then levels ofX Although not shown, the same tendency is also seen when 2 vs Furthermore, integration is always positive, at least between 0.6 and 6 Hz, and this is consonant with 3/4 degree flicker data or 8 vs 2 deg flicker data are evidence that photopic flicker sensitivity is enhanced compared, or when similar comparisons were made with data from the other observer. Clearly, at sco- with area increases regardless of frequency when stimulus edges are eliminated (Kelly, 1969a). While in topic light levels, the influences of spatial summation our experiment the flickering disks were sharply is largest for frequencies of about 2 Hz or greater. focussed against a dark background, they were neverDiscussian theless detected only by rods which possess poor high On the basis of the three experiments conducted in spatial frequency sensitivity in comparison with cones (Campbell and Robson, 1968). Therefore, our manippart 1 we conclude that rod vision differs from cone ulation of stimulus size probably resuited more in *For example, assume that about 2% of the steady annular pure area changes than edge position changes. As flux at +O.l log scat. td (i.e. - l.6log Scot. td) were area of stimulation varies between 3/4 deg and 8 deg, scattering onto the locus of Ilicker (at a mean level of therefore, our data again suggest that the scotopic - 1.3log scat. td). Then we would predict (from Fig. 4: temporal frequency response behaves comparably to R.N.) an approx. 0.14 log increase in amplitude inthe photopic response. tensity at I Hz necessary to maintain modulation Like the photopic response, our low-intensity data threshold as annular intensity is raised from -0.2 to f0. I log Scot. td. We would similarly expect a 0.06 log also manifest evidence of frequency-specific behavior increase in amplitude intensity at 7 Hz. From Fig. 5 for frequencies above and below 2-4Hz. First, our (R.N.) it can he seen that the actual increases in frequency response functions are approximately amplitude intensity necessary to maintain threshold when annular intensity is raised from -0.2 to fO.l log band-pass and peak at around 2 Hz. Second, for intensities close to about - 1.3 log scotopic troland, scat. td are 0.15 log for 1Hz and 0.07 log for 7 Hz.

frequencies below 4 Hz manifest Weber-law behavior, those above manifest less compressive behavior. indicative of two possibly distinct mechanisms (Smith. 1973). Third. spatial summation is greatest for flicker frequencies of about 2 Hz or greater. There appears to be evidence, therefore, for differential processing of flicker at rod-mediated intensities over relatively low and relatively high frequency bands. To determine whether these differences signify channeling behavior, Part 2 of our study was performed. PART 2: THE FREQUENCY DEPENDENT NATURE OF FLICKER ADAPTATION

Methods

In these experiments, the observer was presented with an adapting flicker train of constant mean illuminance (- I .3 log scat td) at one frequency and modulation depth for a specified time interval per experimental session. Then the observer adjusted the depth of modulation of the flickering test light (same source) of some specified frequency but of the same mean illuminance to modulation threshold. These two procedures defined an experimental trial. In order to minimize the adapting influence of the test stimulus, all thresholds were collected within 30 set at modulation settings never very much above threshold. We also noted a fairly substantial length of time required to recover from flicker adaptation (about 2-3 min).* This last observation necessitated the inclusion of a 200 set rest period between trials. With both observers, the sequence of data collection was in the order they are presented below. Part A. Adapting train duration. The adapting stimulus was - I .3 log Scot td in d.c. illuminance and was a flicker train of either I or 7 Hz frequency (representing relatively slow or fast flicker) and modulated at 70%. As a control, a steadily illuminated disc was also used. The adapting period was 0, 10, 20, 40, 60, or 100 sec. At the end of the adapting period, the observer adjusted either I or 7 Hz test flicker to modulation threshold via an ascending method of production. A single session comprised one adapting frequency, both test frequencies, and all adapting durations. Presentation of the last two parameters was randomized within the first half-session; the second half-session comprised a counterbalanced (reversed-order) presentation. Three types of experimental sessions were used: in a “homoadaptation” session, 1 Hz adaptation was paired with I Hz test flicker, and 7 Hz adaptation with 7 Hz test flicker; in *In a separate experiment, modulation thresholds to I and 7 Hz flicker following homoadaptation (see following text paragraph) at post-adaptation intervals of 60. 120, and 180 set indicated eventual recovery of modulation sensitivity to within I SE of the mean of the unadapted value. Nevertheless, our use of only one adapting frequency per experimental session together with the randomization and counterbalancing of test frequency and adapting duration was designed lo obviate the effects of any residual adaptation in succeeding trials.

“heteroadaptation” sessions. I Hz was palred Nlth 7 Hz and vice versa: in the “light adaptation” session, test flicker followed adaptation to the stead) light. .A ZOOsec rest period was given between trials. Parts B and C. The frequency dependent nature I!/ flicker adapration. In these experiments, the observer

was adapted to a train of flicker of - I.3 log scat td d.c. illuminance for I min. which the results of Part A above indicated to be sufficient to provide reliable flicker adaptation. The adapting stimulus was I. 3. 5. or 7 Hz. In Part B, modulation depth of adapting flicker was fixed at 70%. In a given experimental session, the adapting frequency was fixed and threshold sensitivity to all test fiicker frequencies was examined. Test frequency presentation was randomized in the first half-session and counterbalanced in the second. For observer R.N., each datum reported below represents 8 observations from 4 experimental sessions and for P.C., 4 observations from 2 experimental sessions. In Part C, the adapting stimuli were equated by a “threshold matching” procedure wherein amplitudes of adapting flicker were all equally above their respective d.c.-adapted modulation thresholds (the dashed function in Fig. 8 for observer R.N. and a similar control function for observer P.C.). This was accomplished by setting adapting flicker amplitude proportional to modulation threshold with the highest amplitude as 7O”j,. For P.C. the amplitudes of all adapting flicker were 0.36 log unit over modulation threshold and the modulation depths for 1, 3, 5, and 7 Hz adapting stimuli were, respectively, 26, 27. 41 and 70%. For R.N. the corresponding values were 0.37 log unit over modulation threshold and the modulation depths for I, 3, and 5 Hz adapting stimuli were, respectively, 29,46 and 70%. Sensitivity to 7 Hz flicker for this subject was deemed insufficient to warrent study. In other respects, Part C involved a procedure identical to part B, above. Results

Figure 7 shows the influence of different durations of flicker adaptation on sensitivity to subsequent test flicker trains of I or 7 Hz. The circles indicate a control condition in which the observer is adapted for the indicated time period to a steady disc of the same d.c. illuminance as the test flicker and show that such adaptation has an essentially constant influence with time on subsequent sensitivity to flicker. The squares represent adaptation to 70% modulation amplitude flicker of the same frequency as the subsequent test flicker, or the “homoadaptation” condition. In general, the longer the exposure to such adaptation, the lower the sensitivity to the subsequent test flicker train. Since the hashmarks indicate 9S% confidence intervals (and hence lack of overlap indicates a significant difference error much smaller than O.Ol), highly significant differences are obtained, except in one case (7 Hz for R.N.), after 60 set exposure to 70% modulated flicker.

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Fig. 7. Influence of adapting train duration on sensitivity to a flickering stimulus of - 1.3 log scat td d.c. illuminance for two subjects. In these experiments, an adapting stimulus was presented for the duration indicated on rhe abscissa. Following this adapting stimulus, the observer adjusted the modulation of the flickering test stimulus to threshold. The test stimulus was either I or 7 Hz (upper or lower sets of functions, respectively), and the adapting stimulus was either a steady stimulus (circles), or 70% modulated flicker of the same (squares) or opposite (triangles) frequency. The hash marks indicate &2 SE. See text for further explanation.

The triangles in Fig. 7 show data obtained after That is, sensitivity to 1 Hz “heteroadaptation.” flicker was obtained after exposure to 7 Hz flicker and vice-versa. Note that this type of adaptation is generally less effective than adaptation with the same frequency. Note also that for both subjects, “homoadaptation” significantly (_+2 SE of the mean) depresses sensitivity at 60sec for a 1 Hz test. Only one subject (P.C.), however, showed a significant depression at 60 set for a 7 Hz test. Because no additional depression of sensitivity was apparent for longer *In Fig. 8 for observer R.N., each datum represents the mean of 8 observations. For these data, the analysis of variance showed an interaction between the factors of test and adapting frequency which was highly significant (P < 0.005). Similar data for observer P.C. represent a mean of only four observations. and the interaction between the factors of test and adapting frequency was reduced in significance (P < 0.1).

durations of exposure, we decided to study flicker adaptation using a 60 set adapting interval. In the experiments portrayed in Figs 8-11, the influence of I min flicker adaptation to I, 3, 5, and 7 Hz upon sensitivity to all frequencies of flicker were compared. Sample data for observer R.N. are shown in Fig. 8. These data were obtained when all four adapting trains were fixed in modulation depth at 70%. Once again, modulation sensitivity is plotted as a function of flicker frequency. The small closed symbols indicate data obtained after one minute exposure to a nonflickering stimulus, while the other four symbols indicate data obtained after adaptation to the four indicated flicker frequencies. Clearly, flicker adaptation to any frequency generally depresses flicker sensitivity. In addition, some signs of specificity are shown. That is, 1 and 3 Hz adaptation have a larger influence on flicker sensitivity for frequencies under 3 Hz than do 5 or 7 Hz, while the opposite is true for test frequencies over 3 Hz. This observation was supported by a two-factor analysis of variance.* Although not illustrated, the same tendencies are apparent in the data of the other subject. In order to ascertain the possibility of frequencyspecific adaptation, however, we found further graphic treatment necessary. In Fig. 9, the effect of the four different adapting frequencies (along the ordinate scaled in dB units) are plotted as a function of test flicker frequency. The separate ordinates indicate, individually, the d.c.-comparative sensitivity changes obtained with adapting flicker, while the two different symbols show all such derived data from the two observers used. For both observers, it is clear that 1 Hz adaptation maximally depresses sensitivity to the lowest frequencies, 3 Hz adaptation the middle

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Fig. 9. The change in flicker sensitivity resulting from 60 set of adaptation to 70% modulated Bicker. The four separate plots represent data obtained following exposure to flicker trains of the specified frequencies. Solid line functions represent data from observer R.N. which are plotted in Fig. 8 while dashed-line functions are from similar data of P.C. The ordinate shows the relative sensitivity [in dB = (20)log sensitivity ratio] following flicker exposure in comparison to the sensitivity following exposure to a nonflickering stimulus. The abscissa indicates test flicker frequency.

frequencies, and 5 and 7 Hz flicker, the higher test frequencies. Comparison of the two lower coordinates shows, however, that for observer R.N., 5 Hz adaptation has a greater influence than 7 Hz on sensitivity to all test frequencies indicating, perhaps, that 5 hz falls closer to the peak sensitivity of a “high” frequency channel than 7 Hz. The same general tendency is seen, but less clearly, for observer P.C. The results of Fig. 9 suggest the possibility of frequency channeling in scotopic flicker sensitivity, although the lack of precision in the data preclude all but the most general description. There is an indication in Fig. 9 that the maximum sensitivity depression (minimum adaptation ratio) shifts to higher frequencies as adapting frequency increases from 1 to 7 Hz. This suggests parallel or channeled tuning. On *The data from which Figs 9-1 I were derived (functions similar to Fig. 8) were also analyzed statistically. An analysis of variance again showed an interaction between the factors of test and adapting frequency which was highly significant for observer R.N. (P < 0.005) and

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the other hand, the fact that 7 Hz adaptation is quite weak indicates, perhaps, that tuning is limited to a fairly narrow range of frequencies. In order to clarify our results, the experiments summarized by Figs 8 and 9 were repeated with both observers. This time, however, the modulation depths of the adapting stimuli were “threshold-matched” according to the procedure specified in the methods section in order to more nearly equate the amplitude component of their supra-threshold adapting effects. This was done in the hope of further isolating the frequency component of flicker adaptation. Results from this experiment are shown in Fig. 10. These data show that 1 Hz adaptation has a predominant influence on test flicker frequencies under 2 Hz. The other three adapting frequencies have a predominant influence at 4 Hz.* To emphasize the similar influence of 3,5, and 7 Hz adaptation, some of the data in Fig. 10 are replotted in Fig. I I. This time, the plotted points represent the means of the data from both observers at test frequency values common to both. The connecting lines either pass through the 1 HZ data (dashed lines) or are the means of the 3, 5, and 7 Hz data (solid lines). This plot extends the analysis of Fig. 10 and suggests that the influence of 1 Hz flicker adaptation is unique, while the influence of 3, 5, and 7 Hz adaptation are very similar. Using this approach we find a maximum 3 dB suppression of sensitivity centered at either the adapting frequency for 1 Hz

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Fig. 10 in which the indicated points are the means of data from both observers. The dotted Function passes through the I Hz data, but the solid function represents the mean of the 3. 5, and 7 Hz data. See text for further explanation. adaptation or at 4 Hz for higher frequency {mean of 3,5, and 7 Hz) adaptation. There is at best (averaging the results of two subjects) perhaps a + 1.5 octave half-adaptation bandwidth for 1 Hz adaptation (assuming a symmetrical function) and a It 1.0 octave bandwidth for the higher frequency group. In lieu of a better technique for equating adapting stimuli in terms of the sensitivity of the presumed underlying channels, it is impossible to say how many channels are mediating the adaptation effects. Nevertheless, this plot suggests that the essentials of our scotopic frequency adaptation data appear to be approximately described in terms of the action of two temporal channels.

DlSCUSSION

Selective adaptation is an approach that has been proposed as providing qualified evidence for the existence of sensory channels, especially in the spatial frequency domain (see Braddick et al., 1978). Using sinusoidal gratings (e.g. Regan and Beverley, I983), similar adaptation techniques have produced sensitivity depressions of 8-12 dB (compare with our value of 3 dB) with a half-adaptation bandwidth of 2 1.0 octave (frequency tuning) and +, 14” (orientation tuning). Compared with these reports, our results appear not to be so nearly conclusive of temporal channeling in scotopic vision. Nevertheless, the suggestion in our data of two uniquely adaptable frequency ranges (1 Hz vs 3, 5, and 7 Hz) can be related to photopic discrimination experiments (Watson and Robson. 1981) where distinct temporal frequency detectors have been proposed to operate over either a low (O-2 Hz) or high (8-32 Hz) frequency range. Perhaps these photopic tuning functions are preserved and scaled to a lower frequency range at scotopic levels.

12.5

Our selective adaptation results extend those of previous workers both at photopic levels (Smith, 1970, 1971; Pantle, 1971; Nilsson et al., 1975; Hanley and MacKay, 1979, Cameron, 1982) and levels down to about 1 td (Smith, 1971). We have demonstrated adaptability at levels more than I log unit lower than this. Therefore, in agreement with a recent finding of Conner (19821, we conclude that at least two different channels mediate scotopic flicker sensitivity. Unfortunately, the present frequency adaptation data are too variable and the data of Conner (1978, 1982; Conner and MacLeod, 1977) are sufficiently nonparametric to provide any definite conclusion regarding the number of channels mediating scotopic flicker sensitivity. The existence of multiple rod-channels, however, is not only suggested by temporal frequency adaptation experiments. For exampte, although it is well known that human rods are capable of differentially responding over a range of illuminance levels from absolute threshold up to about 1000 td (Aguilar and Stiles, 1954), at least one type of rod signal often saturates at much lower levels of illuminance. Whittle and MacLeod (as reported by MacLeod, 1974) found that rods only contribute to brightness sensations up to illuminance levels of about 1 Scot. td; simiiarly, Bauer et ai. (1983) found that the rod influence on cone-mediated increment thresholds saturates at about 1 Scot. td. It is important to note that this same value falls close to the upper limit of the “rod plateau” seen in classical flicker data which examined the influence of illuminance on CFF (e.g. Hecht and Schlaer, 1936; also see our fig. 2b). One scotopic troland also represents the saturating limit of the slower of the two rod temporal channels observed by Conner and MacLeod (1977), as well as a point of abrupt transition in increment threshold sensitivity {Conner, 1978). It is therefore likely that I Scot. td demarcates the operation of two rod processes. Since there is no exclusive rod-related pathway to the brain, it is also possible that the present evidence for slow and fast flicker channels in fact represents a distinction between channels that are common to rods and cones as suggested by the data of Smith (1971) and Tyler (1975). Furthermore, we have recently shown that unstimulated, dark adapted rods inhibit high frequency {over 15 Hz), cone-mediated flicker sensitivity, but have only a small influence on slow (under 5 Hz) cone-mediated sensitivity or, indeed, on cone threshold (Goldberg et al., 1983; also see Wooten and Butler, 1976). Finally, it is apparent that several chromatic and at Ieast one achromatic channel have unique temporal response functions (deLange, 1958b; Kelly, 1962; Kelly and van Norren, 1977). UnfortunateIy, we are unaware of any evidence which indicates the relationship of these chromatic channels to putative temporal channels. That is, although counterphase flicker experiments have demonstrated the temporal properties of chromatic channels, no data have yet

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suggested the chromatic properties of putative temporal channels. If common rod-cone pathways contributed to our findings of temporal channeling in scotopic vision. then we might ask what chromatic properties these channels possess. The present results suggest that low and high frequency rod-mediated flicker sensitivities have several unique properties most probably representing the functioning of distinct channels with distinct time constants of response. At least two types of interrelated questions, however. remain to be answered. First, are these distinct channels unique to rods or are they common rod-cone channels? Second. what is the relationship of any putative temporal channels to the chromatic and achromatic channels of color theory? REFERENCES

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