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Comparison of human visual cortical potentials evoked by stabilized and unstabilized targets
visionRer.Vol. 11.pp.657-670.Pergamon Press1971.Printedin Great
Britain.
COMPARISON OF HUMAN, VISUAL CORTICAL POTENTIALS EVOKED BY STABILIZED AND UNSTABILIZED TARGETS’ s2 ULKER TULUNAYKEE~EY OphthalmologySection, Medical School, University of Wisconsin, Madison, Wisconsin 53706, U.S.A. (Received 4 July 1970; in revised form 7 October 1970)
THE PURPOSEof this experiment was to describe the properties of the averaged occipital potential evoked by a small sinusoidally flickering field and to determine if any aspect of the visual evoked cortical potential (VECP) reflects the stabilization of an image on the retina. As it is known so well, when the image on the retina is stabilized so that it cannot shift from one set of receptors to another, the target pattern gradually fades and finally disappears. The physiological basis of this change in the visibility of the stabilized image is not well understood. It seems reasonable to assume that disappearance is the result of adaptation of the activity of the visual system incurred by the stationary image. Indeed, recordings on animal preparations have always shown that an image stationary on the retina leads to a decline in response strength measured either at the peripheral (e.g. HARTLINE, 1938) or central cites (BURNS, HERON and PRITCHARD, 1962); and movements of the retinal image such as would be induced by the normal motions of the eye result in bursts of activity. However, evidence from two studies (RIGGS and WHITTLE, 1967; LEHMANN,BEELERand FENDER,1967) published so far, suggests that in man there is no reduction in the amplitude of the averaged evoked electrical activity of the visual system when the image is stabilized on the retina. In the RIGGS and WHITTLE(1967) study, a grating pattern was stabilized; the electroretinogram and the occipital potentials were evoked by changing each stripe in the grating from black to white and back again. A high enough frequency of shift was chosen so that the grating pattern faded and disappeared easily. However, this subjective effect was not reflected as a reduction of evoked potentials; the amplitude of both the averaged ERG and the EEG remained the same whether the target was viewed under stabilized or normal, unstabilized conditions. They suggested that image disappearance is not related to neural activity generated by the temporal aspects of the stimulus. The LEHMANNet al. experiment (1967) in which occipital potentials were evoked by repetitive flashes presented to one eye while the other eye viewed a target, indicated that averaged potentials occurring during 1This project received support from a National Institutes of Health Grant NB-06151 and from a Genera1 Research Support Grant to the University of Wisconsin Medical School from the National Institutes of Health. Division of Research Facilities and Resources. Part of data analysis was made possible through the Laboratory Computing Facility, University of Wisconsin. 2 I thank Dr. D. WATTS, of the Statistics department, University of Wisconsin, Mr. R. M. JONES and Mr. B. CUTrING for their generous help in the analysis of the data. 657
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stabilized viewing are actually larger than those produced under unstabilized conditions. The technique of signal averaging, which was necessary to separate the small amplitude evoked potentials from the ongoing background activity, did not reveal whether or not any temporal changes such as would be expected if adaptation were taking place occurred in the amplitude of evoked potentials. Several recent studies relate the components of the ongoing electroencephalogram to changes in the visibility of the stabilized image. It was found, for example, that stabilized vision is characterized by an abundance of alpha activity, generally associated with minimal visual input and that alpha can be relied upon to precede the subjective disappearance of the target (LEHMANN,BEELERand FENDER,1965; KEISEY and NICHOLS, 1967; and KEE~EYand NICHOLS,1969). Although this evidence is in favor of centrifugal controi in regulating the disappearance of the stabilized image, it does not exclude the possibility of adaptation of retinal and/or central activity evoked by an image when it is motionless on the retina. The present experiments represent an attempt to characterize and compare cortical activity evoked by a stimulus during stabilized and unstabilized viewing by (1) describing the properties of the cortical potential evoked by a wide range of frequency and amplitude of light variation, (2) by examining the changes of VECP amplitude as a function of time, and (3) by relating the changes of VECP to the changes in the ongoing EEG activity level. Sinusoidal flicker where light in a field varies around a constant average level, was chosen as the stimulus to evoke the occipital potentials. The advantage of this type of stimulus is that the retinal adaptation level remains constant for all frequencies and amplitudes of light variation. In addition, there are data (VAN DER TWEEL and SPEKREIJSE,1966) showing that a large range of modulation amplitudes evokes reliable cortical potentials. Furthermore, in our experience, small sinusoidally modulated fields disappear under stabilized vision if they are viewed for 30 set or more. It seemed appropriate, therefore, to attempt to use a small sinusoidally modulated field in a situation where both image disappearance and evoked potentials are desired. In this study occipital potentials were obtained under both stabilized and normal, unstabilized, viewing conditions, and studied by the computer averaging and spectral analysis techniques. METHOD A 2” sharpedolsd dark surround field such as those frequently used in stabilized image studies, was the
target. It flickered sinusoidally around a constant average luminurce of 80 mL. ModulaGon depths between Oaml100gaantof~a~kvel,anda~offnquarcicsbstw;asnOand60Hzwereavaifable.An artifkial pupil with a diameter of 2.8 mm insured constant r&al &ninancc. Stabilization was acbkved by an optical lever system and the same system was also used for the unstabilized viewing condition that permitted the image to move over the retina in the normal manner. The apparatus used to produce both sinusoidal modulation and imap stabilization has ban descrii elsewhere (ICIWW,1970). The ekctrocncephakgram was picked up by two electrodes, one applkd to the midline vertex, the other 2 cm above and to the right of the inion. It was continuously monitored on a Beckman @nograph, and regkWcdonanFMtaperec0rderforpartoftite cxperbncnt. A Fabri-talcsignal aWager was used at all times to extmct the small amplitude evoked poasatial from the ongoing EEG. The averaging operation was synchronized with a pulse occur&g at the trough of the sinewave stimulus. In a single recording session which lasted approximateiy 30 min. the target was viewed under both stabilizai and unstabilized an&ions. An attempt was made to en6u~ comparibility of the two viewing condirions by equating the quality and lm of the stab&ad and the normally vkwed images. The shatpncmoftheadgeswascompamdbyproj&ng&m&anaou4 ythetwoimagesbymeatzsofamethod dssar’bad~~s,RA~~dKBBpey(l%1).TRclpQulllityQc~l~ofthe~deMswasc~~ at the b&ming of each session by obtaining measuns of flicker fusion fqucncy (at 100 per cent modulation) under the two viewing conditions.
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To reduce the possibility of recording responses of the auditory system to the noise of the motor used to generate flicker, the subject was presented with constant white noise through a pair of padded earphones. In addition, at the beginning and the end of each session, EEG was recorded and averaged when the field flicker was at 0 per cent modulation, that is, when all the machinery to produce flicker was operating, but the field was evenly illuminated. The experiment was done in two parts. In the first, the range of frequencies which yielded an easily distinguishable evoked potential under both viewing conditions was determined. In the second part, a few selected frequencies were presented at various modulation depths for a period of 3 min for the purpose of studying long term progressive changes in response amplitude. One male and two female subjects participated in the’ experiment. One DJN, had continuous large amplitude (40 pV) alpha, the others, UTK and SJL had small amplitude (20 pV) alpha bursts well separated by the tow voltage, high frequency activation pattern. RESULTS
Part I In the first part of the experiment, the modulation amplitude was held constant at 100 per cent and the frequency varied from 3 Hz to a value at which the averaged EEG could no longer be distinguished from the EEG obtained when the subject viewed the steadily illuminated target. The critical fusion frequency for the VECP was 46 Hz for UTK and 41 Hz for SJL. These frequencies corresponded to the point at which the subjects could no longer report flicker. For DJN, the subject with continuous alpha, the CFF for the VECP was 18.5 Hz, he could discriminate flicker up to 50 Hz, however. No explanation could be found for the failure to record from DJN potentials produced by high frequency flicker. Other characteristics of the averaged evoked potential were similar for all three subjects. Both UTK and DJN reported clear visibility of the stabilized image when flicker was below 18.5 Hz. Some disappearance was reported at 185 Hz; at higher rates of flicker the contours of the image faded easily, and sometimes flicker itself disappeared. No data were obtained under the stabilized conditions from SJL, who was not, at that time, fitted with the tight contact lens necessary for image stabilization. All the data from the three subjects were analyzed by the same methods with similar results. Because the data of UTK is the most extensive, the graphical presentation is limited to this subject. Figure 1 presents a sample of the averaged VECP obtained under both viewing conditions for some of the frequencies ranging between 3 and 51 Hz, used in the experiment. Traces depicting the sinusoidal stimulus and the trigger pulse are also shown for each group of responses. Because the sweep speed of the averager was adjusted so that several cycles of sinusoidal flicker could be viewed, and the magni~cation of the display varied for maximum clarity, neither the time nor the ampIitude scale is directly comparabie between each block of four tracings. It is apparent from Fig. 1 that the potentials evoked by sinusoidally flickering light are not always of the same frequency as the stimulus. This non-linearity of the response becomes especially apparent for low flicker frequencies and under the stabilized viewing conditions. As an extreme example, note that stimulation frequencies of 9 and 13 Hz produce, when the image is stabilized, a response composed mostly of the second harmonic. The data from the other subjects confirm these observations. To obtain a rough estimate of the harmonic content of the response, a Fourier analysis (DOEBELIN,1966) was performed on the averaged VECP corresponding to a single cycle of stimulation. Figure 2 summarizes the results of the Fourier analysis on UTK’s data. The evoked potential to all frequencies of stimulation appeared to be composed of the fundamental and the second harmonic under both viewing conditions. Under the stabilized
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unstabilized stabilized stimulus trig. pulse
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condition the magnitude of the third and fourth harmonic seems to be 10 per cent of the fundamental and/or the second harmonic, whereas the higher harmonics under the normal viewing conditions appear to be less than 5 per cent of the significant frequency. In order to estimate the amplitude of the whole potential, the total RMS voltage was calculated. These values were then plotted as a function of stimulus frequency as shown in Fig. 3. It appears that under unstabilized viewing conditions, RMS voltage or the amplitude of the whole VECP decreases with an increase in frequency above 7 Hz. Analysis of !&K’s data obtained under the unstabilized conditions over the whole frequency range and DJN’s data available for frequencies between 3 and 18.5 Hz yielded the same results. Figure 3 shows that when the image is stabilized, the RMS value tends to stay constant up to a frequency of 25 Hz, after which it shows a decline. The most noteworthy feature of Fig. 3 is the difTerence in the RMS values of the potentials elicited by low frequency flicker (3-13 Hz) under the two viewing conditions. A simiIar plot of the total RSM voltage of the VECP obtained from DJN also indicated that when flicker rate is below 18.5 Hz, stabilized vision, i.e. the absence of image movements, yields a smaller potential than unstabilized vision, even though at these low frequencies, the stabilized and the u~tabilized images are seen with equal clarity. However, judging from UTK.‘s data in Fig. 3, flicker frequencies higher than 18.5 Hz result in potential amplitudes which
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FIG. 2. This figure summarizes the results of a Fourier analysis performed on the potential evoked by 1 cycle of flicker. The black bars represent the amplitude of each of the components of the unstabilized, the open bars the stabilized VECP. The amplitude of light modulation was 100 per cent.
show no consistant differences between the two viewing conditions, although as noted before, the stabilized image disappears reliably at these high frequencies of flicker. An attempt was made to determine the phase shift characteristics of the fundamental and the second harmonic of the VECP. There were ambiguities, however, because of too few data points for the low frequencies. Nevertheless, the data from the two subjects who viewed the image under both the stabilized and unstabilized conditions tend to show that the latency of the stabilized VECP (first and second harmonic) was consistently longer than the unstabilized VECP. SO* unslobilizrd
FIG. 3. The total RMS voltage of the VECP is shown as a function of frequency of sinusoidal light modulation. (p) Depicts VECP voltage under unstabilized, (- - - -) stabilized viewing conditions.
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Part ZZ
In the second part of the experiment four frequencies; 7, 13, 18.5, and 26 Hz, representative of the amplitude vs. frequency curves (Fig. 3), were presented at modulation amplitudes of 6, 12, 25, 50 and 100 per cont. Each frequency and amplitude combination was viewed for 3 min under both the stabilized and unstabilized conditions. Two subjects, UTK and DIN, participated in this part of the experiment. They reported complete disappearance of both the contours of the circular field and the flicker at 26 Hz and occasional fading at 18.5 Hz even at high modulation amplitudes of 50 or 100 Per cent. On the other hand, there was no disappearance at all for the lower frequencies, even when modulation amplitude was low. Figure 4 illustrates the three general findings common to both subjects: (I) the averaged VECP for both uns~bi~d and stabilized vision becomes more sinusoidal as modulation amplitude decreases, (2) the log RMS value of the po~n~al increases in an approximately linear fashion with an increase in log modulation amp~tude for both viewing conditions, except at 7 Hz, and (3) the difference between the amplitudes of the stab&& and the unstabilized VECP becomes ambiguous as the modulation amplitude is lowered. 13 Hz
un8toWzed .a-.. rtabfiind Fw. 4. The left hand cobmn shows traciutg of the weraged VECF obtainad de UZKMS)vic&4of 13 ~~at~~~~ )&WAStabilizA (---izedG--amplitudes. The right hand wluma shws toW RMS ~&age of Potentials mmked 6y I@*% 13 and 7 Hz flicker as a function of amplitude of modulation.
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The consistently lower amplitude of the VECP obtained under the stabilized conditions at low frequencies and high modulation amplitudes may be due to a process during which a decrease of potential amplitude occurs over time. The possibility also exists that evoked potentials under stabilized conditions may somehow be modulated by the ongoing EEG which is known to contain more alpha activity under the stabilized than the unstabilized conditions. In order to gain an assessment of the time-dependent changes of the VECP amplitude, . and its relation to the activity level of the ongomg EEG, the 3 min recording was analyzed, first, by averaging the EEG signal for short overlapping intervals, and secondly, by obtaining the power spectrum of the EEG, again for short subdivisions of the entire 3 min recording. The initial 10-12 set, section of each 3-min long EEG was divided into 1.2-25 set intervals, each overlapping the previous one by half its duration. The length of each interval was determined for each frequency by the smallest number of sweeps necessary to obtain an averaged potential. The EEG obtained while viewing the 100 per cent and 50 per cent modulated flicker was used for the analysis, because only for these high amplitudes of modulation was the response large enough to permit substantial improvement of the signalto-noise ratio within a short period of time.
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12 set of viewing. The 12 set interval was divided into nine segments each approximately Represents the unstabilized, 2.5 set and overlapping the previous one by 1.2 sec. (-) (- - - -) stabilized viewing condition. The target was modulated at 100 per cent with a frequency of 18.5 Hz.
The averaged VECP for each of the overlapping intervals was subjected to Fourier analysis. The total RMS voltage of the response waveform for each consecutive overlapping interval gave an indication of the change in VECP amplitude within the first IO-12 set of viewing. A typical result is shown in Fig. 5 for 185 Hz flicker modulated at 100 per cent. Within the limits of this analysis there appears to be no systematic decline in potential amplitude as a function of time, whether or not the image is stabilized. On the other hand, as Fig. 5 shows once more the potential evoked by the stationary retinal image tends to be smaller, even in the first few seconds of viewing, than the response evoked by the
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ULKERTIJLIJNAYKEFSEY
normally moving retinal image when modulation amplitude is high. (Significance level of O-05 < p c O-02 by t test for correlated means for 100 per cent modulation of 18.5, 13 and 7 Hz, and 50 per cent modulation of 18.5 Hz flicker for UTK; p > 0.1 for 100 per cent and 50 per cent modulation of 13 and 7 Hz flicker for DJN.) To obtain an indication of long term changes in potential amplitude and its relation to the ongoing EEG, the entire 3-min EEG sample was divided into 1Zsec sections, each overlapping the previous one by 4 sec. Each 12 set segment was then subjected to a spectral analysis (JENKINSand WAITS, 1969). This analysis gave an estimate of total average power of EEG for all frequencies up to 60 Hz within each of the 12 set segments. Power at each EEG frequency with 05 Hz intervals within the same 12 set segment was also determined and expressed as a percentage of average total power. (Average power is defined as it is in
Comparisonof Human Visual Cortical Potentials
665
communication engineering practice as power dissipated by a voltage, here measured at the electrodes on the skull, across a I- 0 resistor.) Figure 6A shows the power density spectrum EEG for four overlapping 12 set intervals taken from the beginning of the 3 min long recordings. The data represented here were obtained under the control conditions in which a steadily illuminated field having the same average luminance as the flickering field was viewed. The prominent peak here is in the 11*5-12.0 Hz interval, the alpha frequency for this subject. Figures 6B and 6C contain the power spectrum of EEG for four corresponding 12 set intervals of data obtained when the subject viewed a stabilized (Fig. 6B) or an unstabilized field (6C) flickering at 18.5 Hz with a modulation of 100 per cent. As expected, when the field viewed under either condition flickers, peaks appear in the power density spectrum of EEG in the 18-19 Hz interval, which includes the frequency corresponding to that of the flicker. Figure 6B shows that when the image is stabilized, consistent peaks also occur around the EEG frequency of 37 Hz which corresponds to the second harmonic of the flicker frequency. This finding agrees with the previous observation that the stabilized flickering field tends to produce VECP containing more harmonics than its unstabilized counterpart. An indication of progressive changes of power at any EEG frequency can be obtained when the power at that frequency is plotted as a function of the overlapping intervals. The EEG frequencies of interest were those which showed a peak in the power density spectrum, that is, the alpha frequency, and, of course, the frequencies corresponding to the fundamental and the harmonics of flicker frequency, which constitute the evoked potential. Figures 7 and 8 represent such treatment of the EEG data, which were obtained while viewing 100 per cent modulated flicker of 18.5 (Fig. 7) and 13 Hz (Fig. 8) under stabilized and unstabilized conditions. Total average power, and relative power of EEG at 18.5 Hz (Fig. 7) and 13 Hz (Fig. 8) and in addition, the alpha frequency are plotted for each of the 12 set intervals. Although the data obtained when the field was modulated at 6 per cent do not belong on these graphs, they are shown here for the purposes of a cursory comparison. Figures 7 and 8 are representative of an important trend which emerged from the examination of all the data for each of the frequency and amplitude combinations of flicker for each of the two viewing conditions for both subjects. Total average power, that is, the average level of EEG, remains somewhat constant over the 3 min viewing period. It remains at approximately the same level regardless of the viewing conditions and the frequency and amplitude of flicker. This permits comparison of relative power of EEG at any frequency between various stimulus conditions. The main finding concerns the relation of the evoked potential, as indicated by the power of EEG frequencies corresponding to the stimulus frequency and its harmonics, to the average total EEG activity, and to the alpha frequency. Examination of Figs. 7A and 8A shows that when the image is moving normally on the retina, the relative power of EEG at 18.5 or 13 Hz, varies through a large range over the 3-min period. This is true, however, only for flicker modulated at 100 per cent under the unstabilized conditions. Reducing flicker modulation amplitude (Figs. 7A and 8A, 6 per cent modulation) or stabilizing the image (Figs. 7B and 8B), reduces the range of variation. Since power at each frequency is expressed as a percentage of average total power, a wide range of variation over time implies that absolute power at that frequency is independent of the level of ongoing EEG, or average total power. Similarly, a narrow range of variation indicates that absolute power at a particular EEG frequency and total average EEG vary together as a function of time. Indeed, correlation coefficients between EEG power at the frequencies corresponding to the
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Fms. 7A and B. ESG power in each ove&pp& 12 set intervnl is plotted as a function of the in~toBhoWthechanOeof~~inEEOdurinO~3min~~ofan~~(A) ands~~09)tar~.~etotlla~~(P=V’/RwhutR=’l,secturt)~shownas (0 l l l).Thc~in~~~~Garb~~~)containsdintheafphafraqMtcy (x) and 18.5 Hz (0 0 0 0) are also shown. The stimulus was modulated at 100 par cent with ) mts the power at El30 frequency of 18.5 Hz. afrequemyof 18.5 Hz. (---when stimulus frequency was 18.5 Hz and moduktion amplitude 6 per cent. flicker rate, and the average total power were low (r < 0.5) when flicker amplitude
was 100 per cent and the image unstabilized (Figs. 7A and 8A) indicating independence of the evoked potential amplitude from the ongoing EEG level. When modulation amplitudes were 50 per cent and lower (see curves for 6 per cent modulation) and under stabilized conditions regardless of frequency and amplitude of Ilicker, absolute power of EEG at frequencies corresponding to the fundamental (Figs. 7B and 8B) and harmonics of flicker frequency showed strong dependence on the ongoing EEG level (r > 0.8). High correlation between total average EEG and EEG power at frequencies corresponding to stimulation frequencies, may be due to the possibility that level of activity generated by the stimulus and superimposed on the activity already present at that frequency is small; that is, a high correlation actually reflects the dependence of EEG power already present at that frequency on the general EEG level. An attempt was made to estimate the power due to the stimulus alone. From the computer output used to generate Fig. 6, the level of EEG activity was determined for the frequencies immediately preceding, i.e. 180 Hz and following, i.e. 19-OHz, the frequency where the peak activity occurred, i.e. 185 Hz. The average of the EEG power at 18 and 19 Hz was taken as the base level of EEG activity already present at 18.5 Hz. It was then subtracted from the power at 18.5 Hz, the remainder presumably being due to the activity generated by the stimulus alone. This preoedure was repeated for all of the 12 set intervals of the 3 min data and for all of the frequencies of flicker at 100 per cent and 50 per cent
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atcbilized
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3 min OVERLAPPING INTERVALS
FIG. 8A and B. EEG power in each overlapping 12 set interval is plotted as a function of the intervals to show the change of power in EEG during the 3 min viewing of an unstabilized (A) and stabilized (B) target. The average total power (P =V’/R where R = 1 see text)is shown as (0 0 0 l ).The change in relative power(arbitraryunits)contained in the alpha frequency(x) and 13 Hz (0 0 0 0) are also shown. The stimulus was modulated at 100 per cent with a frequency of 13 Hz. (----) Represents the power of EEG frequency of 13 Hz, when the flicker frequency was 13 Hz, and modulation amplitude 6 per cent.
modulation levels for both subjects. Correlation coefficients obtained between the average total EEG and power due to stimulus alone were very low (- 0.3 < r < 0*26), suggesting the independence of EEG activity generated by the flickering stimulus alone from the ongoing EEG level. The relation between the power contained in the alpha frequency and the power contained in the evoked potential, that is, EEG frequencies corresponding to the first or second harmonics of the stimulus frequency, were also examined. The results can be grouped in two categories. (1) Under the unstabilized conditions, overall alpha level for the 3-min period of viewing remains approximately the same regardless of the frequency and amplitude of flicker. Stabilizing the image increases the alpha level approximately two-fold, but only when the flicker frequency is 18.5 or 26 Hz. As it was pointed out before, considerable disappearance of the stabilized image takes place when the image is flickered at these frequencies. At lower frequencies of flicker, 7 and 13 Hz, when no disappearance occurs, the stabilized image produces no increase in the overall alpha level, regardless of the amplitude of flicker. (2) Correlation coefficients were obtained between the power in alpha frequency and the frequencies of the evoked potential (Figs. 7 and 8). They ranged, for all the frequency and amplitude combinations of flicker, between O-4 and 0.9; and showed no
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obvious relation to either the rate or amplitude of light variation or to the two viewing conditions. It appears that the magnitude of the evoked potential does not vary in the same way as does the alpha level. DISCUSSION
AND CONCLUSIONS
The purpose of these studies was to describe and compare the properties of the visual cortical potential elicited under two conditions: (1) when the stimulus, a 2” sinusoidally flickering field, was moving normally on the retina, and (2) when it was stabilized on the retina. The present experiments have shown (as do the studies of VANDER TWEEL and SPEKREIJSE, 1966) that the VECP is not linear under either viewing condition: that is, the potential contains the fundamental and the harmonics of the stimulus flicker frequency. The data suggest that the harmonic content of the stabilized VECP is richer than the unstabilized VECP. The amplitude of the potential measured either by its total RMS voltage, or the amplitude of its fundamental or second harmonic, is a function of both the frequency and amplitude of light variation. The VECP amplitude decreases with an increase of stimulus frequency between 7 and 51 Hz when the image is unstabilized. In the case of stabilized vision, the VECP amplitude remains constant up to 26 Hz. At higher frequencies, stabilized VECP diminishes as does the unstabilized potential. These tidings are reminiscent of psychophysical measurements of threshold for flicker detection (DE LANGE, 1958; KELLY, 1961), which show attenuation of sensitivity to flicker for frequencies higher than 10 or 20 Hz. The log VECP amplitude appears to be approximately linearly related to the log amplitude of light variation under both viewing conditions. The primary finding of the present experiment was that the amplitude of the averaged VECP reflects whether or not the image is motionless on the retina, but only when the frequency of flicker is low, below 20 Hz, and modulation amplitude high, above 50 per cent. It would appear that, under conditions of slow, large amplitude flicker, the normal motions of the image, that is, the stimulation of several sets of receptors by the flickering image, results in the accumulation of cortical activity generated by flicker. In comparison, continuous stimulation of the same receptors by the flickering light, has the net result of a smaller cortical response to flicker. With our methods of analysis, signal averaging and power density functions of EEG over consecutive time intervals, we could find no evidence which would support the suggestion that the diminished VECP of the stabilized viewing condition resulted from a process which shows an orderly decrease of amplitude over time. VECP amplitude was found to vary around a mean level; the range of variation was larger when the image was allowed to move over the retina than when it was stationary. The results indicated that the stabilized VECP settled to a given amplitude level within the first 1-2-23 set of viewing, the smallest time segment we could analyze with our methods. If any adaptation occurred, it must have taken place within this time. The main determiner of the amplitude of the potential evoked by flicker over 20 Hz appears to be the frequency, independent of the presence or absence of image motions. The failure to find any differences in evoked potential amplitude between stabilized and unstabilized conditions by RIGGS and WHI’ZTLB(1967) may be due to the relatively high rates of flicker they employed in their experiments. Neither this experiment nor ours is directly comparable to the experiments by LEHMANNef al. (1967), where a larger VECP was found when the image was stabilized. In the latter experiment, the cortical potentials were elicited by stimulating the right eye by a photoflash while the left eye viewed a stabilized image.
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Although the VECP amplitude indicates the presence or absence of movement of the retinal image under specific stimulus conditions, it is not always a good indicator of either continuous visibility or the disappearance of the image. Here we agree with the results of RIGGS and WHITTLE (1967). The very conditions, low flicker rate and high modulation amplitude, under which the stabilized image yields consistently smaller VECP than the unstabilized image, are also the conditions which are favorable for the maintained clear visibility of the stabilized target. It is true that the conditions favorable for stabilized image disappearance, high rate of flicker, generally produces VECP of smaller amplitudes than a clearly visible stabilized image flickering at a low rate; but, as pointed out before, potentials resulting from flicker over 20 Hz are not consistently different when the image is stabilized and disappearing, than when the image is unstabilized and continuously visible. It appears that for maintainance of seeing, low frequency neural activity is necessary, which is generated either by low rate, high amplitude flicker falling on a given set of receptors or by the movement of the image on several sets of receptors. (See GAARDER, KRAUSKOPF, GRAF, KROPFL and ARMINGTON, 1964.) The modes for generating this low frequency activity seem to be interchangable for continued vision, and the absence of one or the other leads to disappearance. Previous experiments have shown the dependence of stabilized image disappearance on the occurrence of the alpha frequency of the EEG (LEHMANN et al., 1965; KEESEY and NICHOLS, 1967; KEESEY and NICHOLS, 1969). In agreement, the present results show that
alpha is more abundant when flicker rate is high, that is, when image disappearance is likely to occur, than when flicker rate is low. The results also suggest that the VECP amplitude due to flicker is inde~ndent of the general EEG level, and, most impo~antly, from the alpha activity level. It would appear that channels mediating flicker activity are different from those which mediate the disappearance of both contour and the flicker in a stabilized image. REFERENCES BURNS, B. D., HERON, W. and ~~TCHAR~, R. (1962). Physiological excitation of visual cortex in cat’s unanesthetized isolated forebrain. J. Neurophysiol. 25, 165-181. DE LANGE, H. (1958). Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light-I. Attenuation characteristics with white and colored light. J. opt. Sot. Am. 48,777-787. DOEBE~, E. R. (1966). Measurement Systems: Application and Ilesign, McGraw-Hill, New York. GAARDER,K., KRA~SKOPF, J., GRAF, V., KROPFL,W. and ARMING-I-ON, J. C.(1964). Averaged brain activity following saozadic eye move~nt. Science, N. Y. 146,1481-1483. HARTI_IN%H. K. (1938). The response of singleoptic nerve fibres of the vertebrate eye to ill~ination of the retina. Am, J, Physiol. 121,40&-415. JENKMS, G. W. and WATIS, D. G. (1969). SpectraZ Analysis and its Applications, Holden-Day, San Francisco. KEESEY,U. T. and NICHOLS,D. J. (1967). Fluctuations in target visibility as related to the occurrence of the alpha component of the electroencephalogram. Vision Res. 7, 859-879. KEESEY,U. T. and NICHOLS, D. J. (1969). Changes induced in stabilized image visibility by experimental _ alteration of the ongoing EEG. Electroenceph, clin. Neurophysiol. 27, 248-257. KEESEY,U. T. (1970). Variables determining flicker sensitivitv in small fields. J. oDt. Sot. Am. 60.390-398. KELLY,‘D. H. i196l). Visual responses to?ime-dependent stimuli--I. Amplitude sensitivity mdasurements. J. opt. Sot. Am. 51,422-429. LEHMANN, D., BEELERJR., G. W. and FENDER, D. H. (1965). Changes in patterns of the human electroencephalogram during fluctuations of perception of stabilized retinal images. Electroenceph. clin. Neurophysiol. 19, 336-343. LEHMANND., BEELER,JR., G. W. and FENDER, D. H. 61967). EEG responses to tight flashes during the observation of stabilized and normal retinal images. ~lect~aen~eph. cl&. ~europh~~o~. 22, 136-142: RIGGS, L. A. and W~nne, P. (1961). Human occipital and retinal potentials evoked by subjectively faded visual stimuli. Vision Res. 7, 441-451.
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Rrws, L. A., RATLIFF,F. and KBB~BY,U. T.] (1961). Appearance of Mach Eands with a motionless retinal image. J. opt. Sot. Am. 51,702-703. VAN DER TWEW, L. H. and SPEBBBU~B, H. (1966). Visual evoked responses. The clinical value of electroetinography. ZSCERG Symposium, pp. 83-94.
Abatmet-Visual cortical potentials were evoked by a 2” sinusoidally modulated tield. Under both the stabilized and unstabilized conditions, the VECP was composed of the fundamental and the harmonics of the stimulus frequency. The total RMS voltage of the potential was a function of Sicker frequency and amplitude. When Sicker below 20 Hz was used, image stabilization yielded the smaller VECP. There was, however, no subjective disappearance of the stimulus at these low flicker frequertcks. Under either viewing condition fhe VECP amplitude varied randomly as a function of time and did not correlate with changes in either the total EEG level or the alpha frequency of the EEG. R&sum&Gn registre les potentiels visuels du cortex &qt& par un champ de 2” module sinusOIdalernent. A la fols pour des conditions stabill&s et non stabilis&a, le potentiel comprend k fondamental et lea harmoniques da la fr&prence du stimulus. Le voltage quadratique moyen du potentiel total est fonction de la fr@ence et de I’amplitude du papillotement. Pour ks fr6quences inf6rkum.s a 20 Hz, la stabilisation de l’image produit un potentlel mOlmlre. 11 n’y a cependant pas de dlsparition subjective du stimulus a ces basses fr@rences de papillotement. Dans ks det.~ conditions d’obsuvation, l’amplitude des pote&els evoquC varie au hasard en fonction du ternps, sans cOrr&ation ni avec le niveau total de l’ekctroretinogramme ni avec la frtlquence alpha de l’&ctroencephalogramme. -Es wurden SehrindenpOtentiale (S) mit einem zweigradigen sinusoid modulkrten Feld hervorgerufen. S war sow&l bei stabibskrtan aIs such bei unstabilllierten Eadmgungen aus der Eige&equenB und den Oberwelkn der Rei&equenz fllsammengeset~t. Die ganze Etfcktivspannuno war eine Fur&ion der Vem&m&~@ rtquem? u. -amplitude. Eei Flimme&eque.nzen, w&he unter 20 Hz lagen, gab die E&Istabili&ung ein kkineres S. Aber es gab bei dksen &d&en Flimme&equenzen kein subjektlves Verscbwinden des Reizes. In beiderlei Umstinden Pnderte sich die S-Amplitide aufs Geratewohl als Funktion der Zeit und korrelierte weder mit Vergnderungen des gesamten EEG-Niveaus noch der Alphafrequenz des EEG.
Britain.
COMPARISON OF HUMAN, VISUAL CORTICAL POTENTIALS EVOKED BY STABILIZED AND UNSTABILIZED TARGETS’ s2 ULKER TULUNAYKEE~EY OphthalmologySection, Medical School, University of Wisconsin, Madison, Wisconsin 53706, U.S.A. (Received 4 July 1970; in revised form 7 October 1970)
THE PURPOSEof this experiment was to describe the properties of the averaged occipital potential evoked by a small sinusoidally flickering field and to determine if any aspect of the visual evoked cortical potential (VECP) reflects the stabilization of an image on the retina. As it is known so well, when the image on the retina is stabilized so that it cannot shift from one set of receptors to another, the target pattern gradually fades and finally disappears. The physiological basis of this change in the visibility of the stabilized image is not well understood. It seems reasonable to assume that disappearance is the result of adaptation of the activity of the visual system incurred by the stationary image. Indeed, recordings on animal preparations have always shown that an image stationary on the retina leads to a decline in response strength measured either at the peripheral (e.g. HARTLINE, 1938) or central cites (BURNS, HERON and PRITCHARD, 1962); and movements of the retinal image such as would be induced by the normal motions of the eye result in bursts of activity. However, evidence from two studies (RIGGS and WHITTLE, 1967; LEHMANN,BEELERand FENDER,1967) published so far, suggests that in man there is no reduction in the amplitude of the averaged evoked electrical activity of the visual system when the image is stabilized on the retina. In the RIGGS and WHITTLE(1967) study, a grating pattern was stabilized; the electroretinogram and the occipital potentials were evoked by changing each stripe in the grating from black to white and back again. A high enough frequency of shift was chosen so that the grating pattern faded and disappeared easily. However, this subjective effect was not reflected as a reduction of evoked potentials; the amplitude of both the averaged ERG and the EEG remained the same whether the target was viewed under stabilized or normal, unstabilized conditions. They suggested that image disappearance is not related to neural activity generated by the temporal aspects of the stimulus. The LEHMANNet al. experiment (1967) in which occipital potentials were evoked by repetitive flashes presented to one eye while the other eye viewed a target, indicated that averaged potentials occurring during 1This project received support from a National Institutes of Health Grant NB-06151 and from a Genera1 Research Support Grant to the University of Wisconsin Medical School from the National Institutes of Health. Division of Research Facilities and Resources. Part of data analysis was made possible through the Laboratory Computing Facility, University of Wisconsin. 2 I thank Dr. D. WATTS, of the Statistics department, University of Wisconsin, Mr. R. M. JONES and Mr. B. CUTrING for their generous help in the analysis of the data. 657
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stabilized viewing are actually larger than those produced under unstabilized conditions. The technique of signal averaging, which was necessary to separate the small amplitude evoked potentials from the ongoing background activity, did not reveal whether or not any temporal changes such as would be expected if adaptation were taking place occurred in the amplitude of evoked potentials. Several recent studies relate the components of the ongoing electroencephalogram to changes in the visibility of the stabilized image. It was found, for example, that stabilized vision is characterized by an abundance of alpha activity, generally associated with minimal visual input and that alpha can be relied upon to precede the subjective disappearance of the target (LEHMANN,BEELERand FENDER,1965; KEISEY and NICHOLS, 1967; and KEE~EYand NICHOLS,1969). Although this evidence is in favor of centrifugal controi in regulating the disappearance of the stabilized image, it does not exclude the possibility of adaptation of retinal and/or central activity evoked by an image when it is motionless on the retina. The present experiments represent an attempt to characterize and compare cortical activity evoked by a stimulus during stabilized and unstabilized viewing by (1) describing the properties of the cortical potential evoked by a wide range of frequency and amplitude of light variation, (2) by examining the changes of VECP amplitude as a function of time, and (3) by relating the changes of VECP to the changes in the ongoing EEG activity level. Sinusoidal flicker where light in a field varies around a constant average level, was chosen as the stimulus to evoke the occipital potentials. The advantage of this type of stimulus is that the retinal adaptation level remains constant for all frequencies and amplitudes of light variation. In addition, there are data (VAN DER TWEEL and SPEKREIJSE,1966) showing that a large range of modulation amplitudes evokes reliable cortical potentials. Furthermore, in our experience, small sinusoidally modulated fields disappear under stabilized vision if they are viewed for 30 set or more. It seemed appropriate, therefore, to attempt to use a small sinusoidally modulated field in a situation where both image disappearance and evoked potentials are desired. In this study occipital potentials were obtained under both stabilized and normal, unstabilized, viewing conditions, and studied by the computer averaging and spectral analysis techniques. METHOD A 2” sharpedolsd dark surround field such as those frequently used in stabilized image studies, was the
target. It flickered sinusoidally around a constant average luminurce of 80 mL. ModulaGon depths between Oaml100gaantof~a~kvel,anda~offnquarcicsbstw;asnOand60Hzwereavaifable.An artifkial pupil with a diameter of 2.8 mm insured constant r&al &ninancc. Stabilization was acbkved by an optical lever system and the same system was also used for the unstabilized viewing condition that permitted the image to move over the retina in the normal manner. The apparatus used to produce both sinusoidal modulation and imap stabilization has ban descrii elsewhere (ICIWW,1970). The ekctrocncephakgram was picked up by two electrodes, one applkd to the midline vertex, the other 2 cm above and to the right of the inion. It was continuously monitored on a Beckman @nograph, and regkWcdonanFMtaperec0rderforpartoftite cxperbncnt. A Fabri-talcsignal aWager was used at all times to extmct the small amplitude evoked poasatial from the ongoing EEG. The averaging operation was synchronized with a pulse occur&g at the trough of the sinewave stimulus. In a single recording session which lasted approximateiy 30 min. the target was viewed under both stabilizai and unstabilized an&ions. An attempt was made to en6u~ comparibility of the two viewing condirions by equating the quality and lm of the stab&ad and the normally vkwed images. The shatpncmoftheadgeswascompamdbyproj&ng&m&anaou4 ythetwoimagesbymeatzsofamethod dssar’bad~~s,RA~~dKBBpey(l%1).TRclpQulllityQc~l~ofthe~deMswasc~~ at the b&ming of each session by obtaining measuns of flicker fusion fqucncy (at 100 per cent modulation) under the two viewing conditions.
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To reduce the possibility of recording responses of the auditory system to the noise of the motor used to generate flicker, the subject was presented with constant white noise through a pair of padded earphones. In addition, at the beginning and the end of each session, EEG was recorded and averaged when the field flicker was at 0 per cent modulation, that is, when all the machinery to produce flicker was operating, but the field was evenly illuminated. The experiment was done in two parts. In the first, the range of frequencies which yielded an easily distinguishable evoked potential under both viewing conditions was determined. In the second part, a few selected frequencies were presented at various modulation depths for a period of 3 min for the purpose of studying long term progressive changes in response amplitude. One male and two female subjects participated in the’ experiment. One DJN, had continuous large amplitude (40 pV) alpha, the others, UTK and SJL had small amplitude (20 pV) alpha bursts well separated by the tow voltage, high frequency activation pattern. RESULTS
Part I In the first part of the experiment, the modulation amplitude was held constant at 100 per cent and the frequency varied from 3 Hz to a value at which the averaged EEG could no longer be distinguished from the EEG obtained when the subject viewed the steadily illuminated target. The critical fusion frequency for the VECP was 46 Hz for UTK and 41 Hz for SJL. These frequencies corresponded to the point at which the subjects could no longer report flicker. For DJN, the subject with continuous alpha, the CFF for the VECP was 18.5 Hz, he could discriminate flicker up to 50 Hz, however. No explanation could be found for the failure to record from DJN potentials produced by high frequency flicker. Other characteristics of the averaged evoked potential were similar for all three subjects. Both UTK and DJN reported clear visibility of the stabilized image when flicker was below 18.5 Hz. Some disappearance was reported at 185 Hz; at higher rates of flicker the contours of the image faded easily, and sometimes flicker itself disappeared. No data were obtained under the stabilized conditions from SJL, who was not, at that time, fitted with the tight contact lens necessary for image stabilization. All the data from the three subjects were analyzed by the same methods with similar results. Because the data of UTK is the most extensive, the graphical presentation is limited to this subject. Figure 1 presents a sample of the averaged VECP obtained under both viewing conditions for some of the frequencies ranging between 3 and 51 Hz, used in the experiment. Traces depicting the sinusoidal stimulus and the trigger pulse are also shown for each group of responses. Because the sweep speed of the averager was adjusted so that several cycles of sinusoidal flicker could be viewed, and the magni~cation of the display varied for maximum clarity, neither the time nor the ampIitude scale is directly comparabie between each block of four tracings. It is apparent from Fig. 1 that the potentials evoked by sinusoidally flickering light are not always of the same frequency as the stimulus. This non-linearity of the response becomes especially apparent for low flicker frequencies and under the stabilized viewing conditions. As an extreme example, note that stimulation frequencies of 9 and 13 Hz produce, when the image is stabilized, a response composed mostly of the second harmonic. The data from the other subjects confirm these observations. To obtain a rough estimate of the harmonic content of the response, a Fourier analysis (DOEBELIN,1966) was performed on the averaged VECP corresponding to a single cycle of stimulation. Figure 2 summarizes the results of the Fourier analysis on UTK’s data. The evoked potential to all frequencies of stimulation appeared to be composed of the fundamental and the second harmonic under both viewing conditions. Under the stabilized
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unstabilized stabilized stimulus trig. pulse
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condition the magnitude of the third and fourth harmonic seems to be 10 per cent of the fundamental and/or the second harmonic, whereas the higher harmonics under the normal viewing conditions appear to be less than 5 per cent of the significant frequency. In order to estimate the amplitude of the whole potential, the total RMS voltage was calculated. These values were then plotted as a function of stimulus frequency as shown in Fig. 3. It appears that under unstabilized viewing conditions, RMS voltage or the amplitude of the whole VECP decreases with an increase in frequency above 7 Hz. Analysis of !&K’s data obtained under the unstabilized conditions over the whole frequency range and DJN’s data available for frequencies between 3 and 18.5 Hz yielded the same results. Figure 3 shows that when the image is stabilized, the RMS value tends to stay constant up to a frequency of 25 Hz, after which it shows a decline. The most noteworthy feature of Fig. 3 is the difTerence in the RMS values of the potentials elicited by low frequency flicker (3-13 Hz) under the two viewing conditions. A simiIar plot of the total RSM voltage of the VECP obtained from DJN also indicated that when flicker rate is below 18.5 Hz, stabilized vision, i.e. the absence of image movements, yields a smaller potential than unstabilized vision, even though at these low frequencies, the stabilized and the u~tabilized images are seen with equal clarity. However, judging from UTK.‘s data in Fig. 3, flicker frequencies higher than 18.5 Hz result in potential amplitudes which
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FIG. 2. This figure summarizes the results of a Fourier analysis performed on the potential evoked by 1 cycle of flicker. The black bars represent the amplitude of each of the components of the unstabilized, the open bars the stabilized VECP. The amplitude of light modulation was 100 per cent.
show no consistant differences between the two viewing conditions, although as noted before, the stabilized image disappears reliably at these high frequencies of flicker. An attempt was made to determine the phase shift characteristics of the fundamental and the second harmonic of the VECP. There were ambiguities, however, because of too few data points for the low frequencies. Nevertheless, the data from the two subjects who viewed the image under both the stabilized and unstabilized conditions tend to show that the latency of the stabilized VECP (first and second harmonic) was consistently longer than the unstabilized VECP. SO* unslobilizrd
FIG. 3. The total RMS voltage of the VECP is shown as a function of frequency of sinusoidal light modulation. (p) Depicts VECP voltage under unstabilized, (- - - -) stabilized viewing conditions.
ULKER TULUNAY KZESEY
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Part ZZ
In the second part of the experiment four frequencies; 7, 13, 18.5, and 26 Hz, representative of the amplitude vs. frequency curves (Fig. 3), were presented at modulation amplitudes of 6, 12, 25, 50 and 100 per cont. Each frequency and amplitude combination was viewed for 3 min under both the stabilized and unstabilized conditions. Two subjects, UTK and DIN, participated in this part of the experiment. They reported complete disappearance of both the contours of the circular field and the flicker at 26 Hz and occasional fading at 18.5 Hz even at high modulation amplitudes of 50 or 100 Per cent. On the other hand, there was no disappearance at all for the lower frequencies, even when modulation amplitude was low. Figure 4 illustrates the three general findings common to both subjects: (I) the averaged VECP for both uns~bi~d and stabilized vision becomes more sinusoidal as modulation amplitude decreases, (2) the log RMS value of the po~n~al increases in an approximately linear fashion with an increase in log modulation amp~tude for both viewing conditions, except at 7 Hz, and (3) the difference between the amplitudes of the stab&& and the unstabilized VECP becomes ambiguous as the modulation amplitude is lowered. 13 Hz
un8toWzed .a-.. rtabfiind Fw. 4. The left hand cobmn shows traciutg of the weraged VECF obtainad de UZKMS)vic&4of 13 ~~at~~~~ )&WAStabilizA (---izedG--amplitudes. The right hand wluma shws toW RMS ~&age of Potentials mmked 6y I@*% 13 and 7 Hz flicker as a function of amplitude of modulation.
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The consistently lower amplitude of the VECP obtained under the stabilized conditions at low frequencies and high modulation amplitudes may be due to a process during which a decrease of potential amplitude occurs over time. The possibility also exists that evoked potentials under stabilized conditions may somehow be modulated by the ongoing EEG which is known to contain more alpha activity under the stabilized than the unstabilized conditions. In order to gain an assessment of the time-dependent changes of the VECP amplitude, . and its relation to the activity level of the ongomg EEG, the 3 min recording was analyzed, first, by averaging the EEG signal for short overlapping intervals, and secondly, by obtaining the power spectrum of the EEG, again for short subdivisions of the entire 3 min recording. The initial 10-12 set, section of each 3-min long EEG was divided into 1.2-25 set intervals, each overlapping the previous one by half its duration. The length of each interval was determined for each frequency by the smallest number of sweeps necessary to obtain an averaged potential. The EEG obtained while viewing the 100 per cent and 50 per cent modulated flicker was used for the analysis, because only for these high amplitudes of modulation was the response large enough to permit substantial improvement of the signalto-noise ratio within a short period of time.
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12 set of viewing. The 12 set interval was divided into nine segments each approximately Represents the unstabilized, 2.5 set and overlapping the previous one by 1.2 sec. (-) (- - - -) stabilized viewing condition. The target was modulated at 100 per cent with a frequency of 18.5 Hz.
The averaged VECP for each of the overlapping intervals was subjected to Fourier analysis. The total RMS voltage of the response waveform for each consecutive overlapping interval gave an indication of the change in VECP amplitude within the first IO-12 set of viewing. A typical result is shown in Fig. 5 for 185 Hz flicker modulated at 100 per cent. Within the limits of this analysis there appears to be no systematic decline in potential amplitude as a function of time, whether or not the image is stabilized. On the other hand, as Fig. 5 shows once more the potential evoked by the stationary retinal image tends to be smaller, even in the first few seconds of viewing, than the response evoked by the
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normally moving retinal image when modulation amplitude is high. (Significance level of O-05 < p c O-02 by t test for correlated means for 100 per cent modulation of 18.5, 13 and 7 Hz, and 50 per cent modulation of 18.5 Hz flicker for UTK; p > 0.1 for 100 per cent and 50 per cent modulation of 13 and 7 Hz flicker for DJN.) To obtain an indication of long term changes in potential amplitude and its relation to the ongoing EEG, the entire 3-min EEG sample was divided into 1Zsec sections, each overlapping the previous one by 4 sec. Each 12 set segment was then subjected to a spectral analysis (JENKINSand WAITS, 1969). This analysis gave an estimate of total average power of EEG for all frequencies up to 60 Hz within each of the 12 set segments. Power at each EEG frequency with 05 Hz intervals within the same 12 set segment was also determined and expressed as a percentage of average total power. (Average power is defined as it is in
Comparisonof Human Visual Cortical Potentials
665
communication engineering practice as power dissipated by a voltage, here measured at the electrodes on the skull, across a I- 0 resistor.) Figure 6A shows the power density spectrum EEG for four overlapping 12 set intervals taken from the beginning of the 3 min long recordings. The data represented here were obtained under the control conditions in which a steadily illuminated field having the same average luminance as the flickering field was viewed. The prominent peak here is in the 11*5-12.0 Hz interval, the alpha frequency for this subject. Figures 6B and 6C contain the power spectrum of EEG for four corresponding 12 set intervals of data obtained when the subject viewed a stabilized (Fig. 6B) or an unstabilized field (6C) flickering at 18.5 Hz with a modulation of 100 per cent. As expected, when the field viewed under either condition flickers, peaks appear in the power density spectrum of EEG in the 18-19 Hz interval, which includes the frequency corresponding to that of the flicker. Figure 6B shows that when the image is stabilized, consistent peaks also occur around the EEG frequency of 37 Hz which corresponds to the second harmonic of the flicker frequency. This finding agrees with the previous observation that the stabilized flickering field tends to produce VECP containing more harmonics than its unstabilized counterpart. An indication of progressive changes of power at any EEG frequency can be obtained when the power at that frequency is plotted as a function of the overlapping intervals. The EEG frequencies of interest were those which showed a peak in the power density spectrum, that is, the alpha frequency, and, of course, the frequencies corresponding to the fundamental and the harmonics of flicker frequency, which constitute the evoked potential. Figures 7 and 8 represent such treatment of the EEG data, which were obtained while viewing 100 per cent modulated flicker of 18.5 (Fig. 7) and 13 Hz (Fig. 8) under stabilized and unstabilized conditions. Total average power, and relative power of EEG at 18.5 Hz (Fig. 7) and 13 Hz (Fig. 8) and in addition, the alpha frequency are plotted for each of the 12 set intervals. Although the data obtained when the field was modulated at 6 per cent do not belong on these graphs, they are shown here for the purposes of a cursory comparison. Figures 7 and 8 are representative of an important trend which emerged from the examination of all the data for each of the frequency and amplitude combinations of flicker for each of the two viewing conditions for both subjects. Total average power, that is, the average level of EEG, remains somewhat constant over the 3 min viewing period. It remains at approximately the same level regardless of the viewing conditions and the frequency and amplitude of flicker. This permits comparison of relative power of EEG at any frequency between various stimulus conditions. The main finding concerns the relation of the evoked potential, as indicated by the power of EEG frequencies corresponding to the stimulus frequency and its harmonics, to the average total EEG activity, and to the alpha frequency. Examination of Figs. 7A and 8A shows that when the image is moving normally on the retina, the relative power of EEG at 18.5 or 13 Hz, varies through a large range over the 3-min period. This is true, however, only for flicker modulated at 100 per cent under the unstabilized conditions. Reducing flicker modulation amplitude (Figs. 7A and 8A, 6 per cent modulation) or stabilizing the image (Figs. 7B and 8B), reduces the range of variation. Since power at each frequency is expressed as a percentage of average total power, a wide range of variation over time implies that absolute power at that frequency is independent of the level of ongoing EEG, or average total power. Similarly, a narrow range of variation indicates that absolute power at a particular EEG frequency and total average EEG vary together as a function of time. Indeed, correlation coefficients between EEG power at the frequencies corresponding to the
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Fms. 7A and B. ESG power in each ove&pp& 12 set intervnl is plotted as a function of the in~toBhoWthechanOeof~~inEEOdurinO~3min~~ofan~~(A) ands~~09)tar~.~etotlla~~(P=V’/RwhutR=’l,secturt)~shownas (0 l l l).Thc~in~~~~Garb~~~)containsdintheafphafraqMtcy (x) and 18.5 Hz (0 0 0 0) are also shown. The stimulus was modulated at 100 par cent with ) mts the power at El30 frequency of 18.5 Hz. afrequemyof 18.5 Hz. (---when stimulus frequency was 18.5 Hz and moduktion amplitude 6 per cent. flicker rate, and the average total power were low (r < 0.5) when flicker amplitude
was 100 per cent and the image unstabilized (Figs. 7A and 8A) indicating independence of the evoked potential amplitude from the ongoing EEG level. When modulation amplitudes were 50 per cent and lower (see curves for 6 per cent modulation) and under stabilized conditions regardless of frequency and amplitude of Ilicker, absolute power of EEG at frequencies corresponding to the fundamental (Figs. 7B and 8B) and harmonics of flicker frequency showed strong dependence on the ongoing EEG level (r > 0.8). High correlation between total average EEG and EEG power at frequencies corresponding to stimulation frequencies, may be due to the possibility that level of activity generated by the stimulus and superimposed on the activity already present at that frequency is small; that is, a high correlation actually reflects the dependence of EEG power already present at that frequency on the general EEG level. An attempt was made to estimate the power due to the stimulus alone. From the computer output used to generate Fig. 6, the level of EEG activity was determined for the frequencies immediately preceding, i.e. 180 Hz and following, i.e. 19-OHz, the frequency where the peak activity occurred, i.e. 185 Hz. The average of the EEG power at 18 and 19 Hz was taken as the base level of EEG activity already present at 18.5 Hz. It was then subtracted from the power at 18.5 Hz, the remainder presumably being due to the activity generated by the stimulus alone. This preoedure was repeated for all of the 12 set intervals of the 3 min data and for all of the frequencies of flicker at 100 per cent and 50 per cent
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atcbilized
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3 min OVERLAPPING INTERVALS
FIG. 8A and B. EEG power in each overlapping 12 set interval is plotted as a function of the intervals to show the change of power in EEG during the 3 min viewing of an unstabilized (A) and stabilized (B) target. The average total power (P =V’/R where R = 1 see text)is shown as (0 0 0 l ).The change in relative power(arbitraryunits)contained in the alpha frequency(x) and 13 Hz (0 0 0 0) are also shown. The stimulus was modulated at 100 per cent with a frequency of 13 Hz. (----) Represents the power of EEG frequency of 13 Hz, when the flicker frequency was 13 Hz, and modulation amplitude 6 per cent.
modulation levels for both subjects. Correlation coefficients obtained between the average total EEG and power due to stimulus alone were very low (- 0.3 < r < 0*26), suggesting the independence of EEG activity generated by the flickering stimulus alone from the ongoing EEG level. The relation between the power contained in the alpha frequency and the power contained in the evoked potential, that is, EEG frequencies corresponding to the first or second harmonics of the stimulus frequency, were also examined. The results can be grouped in two categories. (1) Under the unstabilized conditions, overall alpha level for the 3-min period of viewing remains approximately the same regardless of the frequency and amplitude of flicker. Stabilizing the image increases the alpha level approximately two-fold, but only when the flicker frequency is 18.5 or 26 Hz. As it was pointed out before, considerable disappearance of the stabilized image takes place when the image is flickered at these frequencies. At lower frequencies of flicker, 7 and 13 Hz, when no disappearance occurs, the stabilized image produces no increase in the overall alpha level, regardless of the amplitude of flicker. (2) Correlation coefficients were obtained between the power in alpha frequency and the frequencies of the evoked potential (Figs. 7 and 8). They ranged, for all the frequency and amplitude combinations of flicker, between O-4 and 0.9; and showed no
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obvious relation to either the rate or amplitude of light variation or to the two viewing conditions. It appears that the magnitude of the evoked potential does not vary in the same way as does the alpha level. DISCUSSION
AND CONCLUSIONS
The purpose of these studies was to describe and compare the properties of the visual cortical potential elicited under two conditions: (1) when the stimulus, a 2” sinusoidally flickering field, was moving normally on the retina, and (2) when it was stabilized on the retina. The present experiments have shown (as do the studies of VANDER TWEEL and SPEKREIJSE, 1966) that the VECP is not linear under either viewing condition: that is, the potential contains the fundamental and the harmonics of the stimulus flicker frequency. The data suggest that the harmonic content of the stabilized VECP is richer than the unstabilized VECP. The amplitude of the potential measured either by its total RMS voltage, or the amplitude of its fundamental or second harmonic, is a function of both the frequency and amplitude of light variation. The VECP amplitude decreases with an increase of stimulus frequency between 7 and 51 Hz when the image is unstabilized. In the case of stabilized vision, the VECP amplitude remains constant up to 26 Hz. At higher frequencies, stabilized VECP diminishes as does the unstabilized potential. These tidings are reminiscent of psychophysical measurements of threshold for flicker detection (DE LANGE, 1958; KELLY, 1961), which show attenuation of sensitivity to flicker for frequencies higher than 10 or 20 Hz. The log VECP amplitude appears to be approximately linearly related to the log amplitude of light variation under both viewing conditions. The primary finding of the present experiment was that the amplitude of the averaged VECP reflects whether or not the image is motionless on the retina, but only when the frequency of flicker is low, below 20 Hz, and modulation amplitude high, above 50 per cent. It would appear that, under conditions of slow, large amplitude flicker, the normal motions of the image, that is, the stimulation of several sets of receptors by the flickering image, results in the accumulation of cortical activity generated by flicker. In comparison, continuous stimulation of the same receptors by the flickering light, has the net result of a smaller cortical response to flicker. With our methods of analysis, signal averaging and power density functions of EEG over consecutive time intervals, we could find no evidence which would support the suggestion that the diminished VECP of the stabilized viewing condition resulted from a process which shows an orderly decrease of amplitude over time. VECP amplitude was found to vary around a mean level; the range of variation was larger when the image was allowed to move over the retina than when it was stationary. The results indicated that the stabilized VECP settled to a given amplitude level within the first 1-2-23 set of viewing, the smallest time segment we could analyze with our methods. If any adaptation occurred, it must have taken place within this time. The main determiner of the amplitude of the potential evoked by flicker over 20 Hz appears to be the frequency, independent of the presence or absence of image motions. The failure to find any differences in evoked potential amplitude between stabilized and unstabilized conditions by RIGGS and WHI’ZTLB(1967) may be due to the relatively high rates of flicker they employed in their experiments. Neither this experiment nor ours is directly comparable to the experiments by LEHMANNef al. (1967), where a larger VECP was found when the image was stabilized. In the latter experiment, the cortical potentials were elicited by stimulating the right eye by a photoflash while the left eye viewed a stabilized image.
Comparison
of Human Visual Cortical Potentials
669
Although the VECP amplitude indicates the presence or absence of movement of the retinal image under specific stimulus conditions, it is not always a good indicator of either continuous visibility or the disappearance of the image. Here we agree with the results of RIGGS and WHITTLE (1967). The very conditions, low flicker rate and high modulation amplitude, under which the stabilized image yields consistently smaller VECP than the unstabilized image, are also the conditions which are favorable for the maintained clear visibility of the stabilized target. It is true that the conditions favorable for stabilized image disappearance, high rate of flicker, generally produces VECP of smaller amplitudes than a clearly visible stabilized image flickering at a low rate; but, as pointed out before, potentials resulting from flicker over 20 Hz are not consistently different when the image is stabilized and disappearing, than when the image is unstabilized and continuously visible. It appears that for maintainance of seeing, low frequency neural activity is necessary, which is generated either by low rate, high amplitude flicker falling on a given set of receptors or by the movement of the image on several sets of receptors. (See GAARDER, KRAUSKOPF, GRAF, KROPFL and ARMINGTON, 1964.) The modes for generating this low frequency activity seem to be interchangable for continued vision, and the absence of one or the other leads to disappearance. Previous experiments have shown the dependence of stabilized image disappearance on the occurrence of the alpha frequency of the EEG (LEHMANN et al., 1965; KEESEY and NICHOLS, 1967; KEESEY and NICHOLS, 1969). In agreement, the present results show that
alpha is more abundant when flicker rate is high, that is, when image disappearance is likely to occur, than when flicker rate is low. The results also suggest that the VECP amplitude due to flicker is inde~ndent of the general EEG level, and, most impo~antly, from the alpha activity level. It would appear that channels mediating flicker activity are different from those which mediate the disappearance of both contour and the flicker in a stabilized image. REFERENCES BURNS, B. D., HERON, W. and ~~TCHAR~, R. (1962). Physiological excitation of visual cortex in cat’s unanesthetized isolated forebrain. J. Neurophysiol. 25, 165-181. DE LANGE, H. (1958). Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light-I. Attenuation characteristics with white and colored light. J. opt. Sot. Am. 48,777-787. DOEBE~, E. R. (1966). Measurement Systems: Application and Ilesign, McGraw-Hill, New York. GAARDER,K., KRA~SKOPF, J., GRAF, V., KROPFL,W. and ARMING-I-ON, J. C.(1964). Averaged brain activity following saozadic eye move~nt. Science, N. Y. 146,1481-1483. HARTI_IN%H. K. (1938). The response of singleoptic nerve fibres of the vertebrate eye to ill~ination of the retina. Am, J, Physiol. 121,40&-415. JENKMS, G. W. and WATIS, D. G. (1969). SpectraZ Analysis and its Applications, Holden-Day, San Francisco. KEESEY,U. T. and NICHOLS,D. J. (1967). Fluctuations in target visibility as related to the occurrence of the alpha component of the electroencephalogram. Vision Res. 7, 859-879. KEESEY,U. T. and NICHOLS, D. J. (1969). Changes induced in stabilized image visibility by experimental _ alteration of the ongoing EEG. Electroenceph, clin. Neurophysiol. 27, 248-257. KEESEY,U. T. (1970). Variables determining flicker sensitivitv in small fields. J. oDt. Sot. Am. 60.390-398. KELLY,‘D. H. i196l). Visual responses to?ime-dependent stimuli--I. Amplitude sensitivity mdasurements. J. opt. Sot. Am. 51,422-429. LEHMANN, D., BEELERJR., G. W. and FENDER, D. H. (1965). Changes in patterns of the human electroencephalogram during fluctuations of perception of stabilized retinal images. Electroenceph. clin. Neurophysiol. 19, 336-343. LEHMANND., BEELER,JR., G. W. and FENDER, D. H. 61967). EEG responses to tight flashes during the observation of stabilized and normal retinal images. ~lect~aen~eph. cl&. ~europh~~o~. 22, 136-142: RIGGS, L. A. and W~nne, P. (1961). Human occipital and retinal potentials evoked by subjectively faded visual stimuli. Vision Res. 7, 441-451.
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Rrws, L. A., RATLIFF,F. and KBB~BY,U. T.] (1961). Appearance of Mach Eands with a motionless retinal image. J. opt. Sot. Am. 51,702-703. VAN DER TWEW, L. H. and SPEBBBU~B, H. (1966). Visual evoked responses. The clinical value of electroetinography. ZSCERG Symposium, pp. 83-94.
Abatmet-Visual cortical potentials were evoked by a 2” sinusoidally modulated tield. Under both the stabilized and unstabilized conditions, the VECP was composed of the fundamental and the harmonics of the stimulus frequency. The total RMS voltage of the potential was a function of Sicker frequency and amplitude. When Sicker below 20 Hz was used, image stabilization yielded the smaller VECP. There was, however, no subjective disappearance of the stimulus at these low flicker frequertcks. Under either viewing condition fhe VECP amplitude varied randomly as a function of time and did not correlate with changes in either the total EEG level or the alpha frequency of the EEG. R&sum&Gn registre les potentiels visuels du cortex &qt& par un champ de 2” module sinusOIdalernent. A la fols pour des conditions stabill&s et non stabilis&a, le potentiel comprend k fondamental et lea harmoniques da la fr&prence du stimulus. Le voltage quadratique moyen du potentiel total est fonction de la fr@ence et de I’amplitude du papillotement. Pour ks fr6quences inf6rkum.s a 20 Hz, la stabilisation de l’image produit un potentlel mOlmlre. 11 n’y a cependant pas de dlsparition subjective du stimulus a ces basses fr@rences de papillotement. Dans ks det.~ conditions d’obsuvation, l’amplitude des pote&els evoquC varie au hasard en fonction du ternps, sans cOrr&ation ni avec le niveau total de l’ekctroretinogramme ni avec la frtlquence alpha de l’&ctroencephalogramme. -Es wurden SehrindenpOtentiale (S) mit einem zweigradigen sinusoid modulkrten Feld hervorgerufen. S war sow&l bei stabibskrtan aIs such bei unstabilllierten Eadmgungen aus der Eige&equenB und den Oberwelkn der Rei&equenz fllsammengeset~t. Die ganze Etfcktivspannuno war eine Fur&ion der Vem&m&~@ rtquem? u. -amplitude. Eei Flimme&eque.nzen, w&he unter 20 Hz lagen, gab die E&Istabili&ung ein kkineres S. Aber es gab bei dksen &d&en Flimme&equenzen kein subjektlves Verscbwinden des Reizes. In beiderlei Umstinden Pnderte sich die S-Amplitide aufs Geratewohl als Funktion der Zeit und korrelierte weder mit Vergnderungen des gesamten EEG-Niveaus noch der Alphafrequenz des EEG.