Ongoing occipital rhythms and the VER. I. Stimulation at peaks of the alpha-rhythm. John L. Trimble and Albert M. Potts

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1 Ongoing occipital rhythms and the VER. I. Stimulation at peaks of the alpha-rhythm John L. Trimble and Albert M. Potts As a first step toward determining the source of variability in the visually evoked response (VER) between subjects, we have eocamined the relationships between the VER and' the a-rhythm. This was done by comparing the VER's to photic stimuli delivered at positive and negative peaks of the a-rhythm (asynchronized stimuli) with VER's to flashes delivered at a fixed interval, unsynchronized with the a-rhythm. Average VER's for the three classes of stimuli were calculated for each of ten subjects. In addition, a grand average VER (GVER) was calculated for each stimulus class by averaging the individual average VER's. Quantitative comparisons between GVER's were made using cross-correlograms. Cross-correlograms were calculated between each of the GVER's, and between the GVER's to asynchronized stimulation and their controls. These data show that the first 120 msec, poststimulus interval of the GVER's to asynchronized stimulation are highly correlated with the prestimulus a-rhythm. The data also show a component occurring in all GVER's which is independent of the a-rhythm. This component begins 120 msec, after stimulation, reaches peak amplitude at 200 msec, and decays to baseline at 240 msec. These findings suggest that much of the variability in VER recordings may be due to a-activity which has been insufficiently attenuated by averaging. Key words: VER, variability, EEG, a-rhythm, human. 0, ur laboratory has concerned itself in the past with several aspects of the visually evoked response (VER), among these the variability of the record from individual to From the Eye Research Laboratories and Department of Ophthalmology, University of Chicago, 950 E. 59 St., Chicago, Supported in part by United States Public Health Service Grant Number EY-00212, from the National Eye Institute, National Institutes of Health, Bethesda, Md., and the L. L. Sinton Trust Research Grant. Submitted for publication July 8, Reprint requests: Dr. J. Trimble, Department of Ophthalmology, University of Chicago, 950 E. 59 St., Chicago, individual and in the same individual from recording to recording It is axiomatic that in any recording made after a light stimulus, from occipital scalp electrodes, part of the record will represent a potential change evoked by the stimulus and reflecting some of the properties of the stimulus, and part of the record will not be evoked from the central nervous system (CNS) by the stimulus (muscle potentials) or will not reflect properties of the stimulus (ongoing electroencephalogram [EEG] activity). Because of the existence of these unwanted potentials all present-day laboratories use some form of algebraic summation of the record, time-locked to the stimulus, to improve signal-to-noise ratio. Indeed, when

2 538 Trimble and Potts Investigative Ophthalmology July 1975 (A) (B) FILTER EEG- s 2] 3 0- z -5" SCHMITT TRIGGER FREQUENCY (HZ) PG-1 PG-2 I 20 FM TAPE STROBE Fig. 1. A, a block diagram of the apparatus used to trigger flash stimuli in phase with the a-rhythm. PG-1 and PG-2 refer to pulse generators producing 2.0 seconds and 10 msec, pulses, respectively. Details are given in text. B, the frequency characteristics of the bandpass filter. -3 db. points are 8 Hz. and 13 Hz. Passband gain is 2.9 db. Attenuation rate is ± 6 db. per octave. Maximum phase error in passband is ± 14 degrees. we write VER these days we tacitly assume that we are referring to such a sum of an unspecified number of responses. We, also, tacitly assume that the potentials not reflecting the properties of the stimulus have been eliminated. The variability that we and many others have observed in the summated records suggests that this is not really the case. It suggests that within the summated potential record which we optimistically label "VER" there lies a series of potential changes which truly reflect the properties of the stimulus and which one might label "ideal VER." If all electrical activity other than the direct response reflecting stimulus properties were truly random, this other electrical activity should indeed be eliminated by the averaging process and "VER" and "ideal VER" should be identical. The observed variability suggests, then, that the unwanted portion of the record, especially after fixed interval stimuli, is not random. A good candidate for the nonrandom potential change is the occipital a-rhythm known to be "driven" by light stimuli. The possibility must be considered, also, that the configuration of the ideal VER may be determined by phase relations between the a-rhythm and the visual stimulus. Others who have considered this possibility are Bechtereva and Zontov, 3 Callaway and Layne, 4 Dustman and Beck, 5 Kooi and Bagchi, 0 and Remond and Lesevre. 7 This is the first of a series of publications which describe our investigation of the problem posed above. Methods Ten adult subjects having normal vision were studied. Subjects were not selected on the basis of the amount or amplitude of a-rhythm in their EEC The subjects sat facing a uniform white hemisphere 0.3 M deep which subtended a visual angle of 106. The hemisphere was illuminated using a Grass PS-22 photostimulator mounted to one side. To insure uniformity of illumination, an opal glass diffuser was placed in front of the strobe. The radiant energy of the full-field flash was 3.9 x 10~ 7 Joules per square centimeter. 0 The subjects' pupils were not dilated. The subjects sat in a darkened electrically shielded room for the duration of the experiment. They listened to white noise through headphones to minimize extraneous auditory stimuli. Each subject first received 50 stimuli presented at regular intervals of two seconds. These were followed by a control where 50 samples were taken at two-second intervals. During each control period, the light flash was occluded by a mask placed before the strobe head. Next, the subject received 50 stimuli presented at negative "The radiant energy of the flash stimulus was measured at 550 nm. (Baird-Atomic interference filter, 22 per cent transmittance, 0.74 optical density) using an EG & G Lite-Mike whose detector head was placed 0.3 m. from the apex of the hemisphere.

3 Volume 14 Number 7 Occipital rhythms and VER 539 peaks of his a-rhythm. These were presented at intervals of no less than two seconds. They were followed by a control where 50 samples were taken at negative a-peaks. Finally, the subject received 50 stimuli coincident with positive peaks of his a-rhythm. These were followed by a control with 50 samples taken at positive a-peaks. The instrumentation used to synchronize the photic stimuli with the a-rhythm is shown in Fig. 1. The EEG was filtered for a-rhythm using a first-order bandpass filter having -3 db. points of 8 and 13 Hz. The filter's passband gain was 2.9 db. and its maximum passband phase error was ± 14 degrees. The filtered EEG was then used to trigger an adjustable threshold Schmitt trigger. Whenever the preset threshold of the Schmitt trigger was exceeded, its output would change from the low (-15 v.) to the high (+15 v.) state. It would remain in the high state until the amplitude of the filtered EEG fell below threshold. The change of state of the Schmitt trigger (low to high) then caused a pulse generator (PG-1, Fig. 1, A) to produce a two-second pulse. The leading edge of this pulse caused a second pulse generator (PG-2, Fig. 1, A) to produce a 10 msec, pulse. This pulse triggered the strobe and was recorded on FM magnetic tape (Sanborn 3917 tape system) to identify the time of stimulation. The two-second pulse from PG-1 insured that stimuli would not be delivered at intervals of less than two seconds, since PG-1 could not be triggered by the Schmitt trigger during production of this pulse. The intermediate outputs of components in this scheme are shown in Fig. 2. The threshold of the Schmitt trigger was set while the subject rested quietly in a darkened room. It was adjusted to produce stimuli during a-activity which was easily discernible above the background noise level. Since an absolute threshold criterion was used, stimuli would sometimes occur on leading or falling edges of the a-cycle instead of peaks due to variations in the peak-topeak amplitude of a-activity. The phase error between time of stimulation and a-peak was no more than ±20. The VER was recorded using a bipolar configuration with ths active electrode placed just above the inion on the midline, and the indifferent electrode placed 3 cm. anteriorly. The earlobe was used as a reference ground. The EEG was amplified by 10 r> using a Grass P511 ACcoupled preamplifier having a bandwidth of 0.3 Hz. to 100 Hz. (-3 db. points). Following amplification, the EEG was recorded on FM magnetic tape along with the stimulus pulses. Subsequent analysis of the recorded data was done using a DEC PDP-15 digital computer. Data were sampled at 250 samples per second, EEG FEEG^^TV HIGH LOW PG-1 PG-2 100mSEC Fig. 2. The intermediate outputs of the components in the a-triggering device of Fig. 1, A. EEG is the raw EEG. FEEG is the filtered EEG (bandpass filter output). ST, PG-1, and PG-2 refer to- the Schmitt trigger, and 2.0 seconds and 10 msec, pulse generators, respectively. When FEEG exceeds the threshold (TH) of the Schmitt trigger, ST changes from the low to the high state. This change initiates a pulse in PG-1 which initiates a pulse in PG-2. Note that PG-1 cannot be triggered while it is producing a pulse. Zero volts is indicated by the dashed line in all traces. The calibration for EEG and FEEG is indicated by the vertical line marked 10 A*V. The time calibration is indicated by the horizontal line marked 100 msec. for 200 msec, prior to, and 1.0 second following stimulation. When average VER's and controls had been obtained for the three types of stimuli, for each of the 10 subjects, a grand average VER was then calculated for each stimulus group and for each control group. Results Fig. 3 shows the average VER's and controls, as well as the grand averages for stimuli presented at fixed intervals. The variability of VER's between subjects can be easily seen in this figure. A possible common point in the average VER's, however, may be the negative (upward) component which reaches peak amplitude 200 msec, following stimulation. The consistency of this component in the average VERs is supported by its appearance in the grand average VER (GAF). In contrast, the average VER's to stimuli presented at negative a-peaks shown in Fig. 4 seem to show more consistency than

4 540 Trimble and Potts Investigative Ophthalmology July 1975 GAF FIXED STIMULUS INTERVAL ""CONTROL GAFCk-W******* DS'* KP Fig. 3. (Left) Individual VER's (designated by subject's initials) and grand average VER (GAF) to flash stimuli occurring with a fixed frequency of one flash per 2.0 seconds. (Right) The individual control averages, and grand control average (GAFC) for this stimulus group. Scales for the ordinates and abscissae of the averages are 4.0 juv per division and 100 msec, per division. Each individual average represents 52 responses. The time of stimulation is indicated by the vertical line at 200 msec, in each plot. Negativity at the inion results in an upward deflection. those to fixed-interval stimuli. With the possible exception of subjects MF and KP, four major deflections can be easily observed in the 200 msec, interval following stimulation. These also appear in the grand average VER for this stimulus group (GAN). The latencies of these peaks in the grand average VER are 52 msec, 96 msec, 124 msec, and 196 msec. A similar consistency in average VER's can also be seen in the responses to stimuli delivered at positive a-peaks shown in Fig. 5. In the 200 msec, following stimulation, nearly all the VER's contain three major deflections. These also appear in the grand average VER for this stimulus group (GAP). The latencies of these peaks are 56 msec, 96 msec, and 204 msec Notice that the peaks at 56 msec and 96 msec, have the opposite polarity to peaks with similar latencies in the grand average VER to stimuli presented at negative a-peaks shown in Fig. 4. A further difference between these two grand average VER's is the absence of a deflection reaching peak amplitude at 124 msec, following stimulation in the grand average VER to stimuli presented at positive a-peaks. Discussion At this point, three questions arise: (1) do the VER's to a-synchronized stimulation show less variability between subjects because a has completely masked the early portions of the "ideal VER." (2) Is the VER component which reaches peak amplitude 200 msec, following stimulation independent of the a-rhythm? and, (3) Does the difference in the number of components between the grand average VER's to a- synchronized stimulation reflect a deterministic relationship between the "ideal VER" and the a-rhythm, or is it merely a consequence of summation of the two signals? We attempted to answer these questions

5 Volume 14 Number 7 Occipital rhythms and VER 541 POSITIVE ALPHA PEAK STTMU LLTS CON T RO L Fig. 4. (Left) Individual VER's and grand average VER (GAP) to flash stimuli synchronized with positive (downward) peaks in the a-rhythm. GAPC designates the grand control average. Details are the same as in Fig. 3. NEGATIVE ALPHA STIMULUS PEAK CONTROL GAN DS Fig. 5. (Left) Individual VER's and grand average VER (GAN) to flash stimuli synchronized with negative (upward) peaks in the a-rhythm. (Right) Control averages, averaging synchronized to negative peaks in the a-rhythm. GANC is the grand control average. For details see Fig. 3.

6 542 Trimble and Potts Investigative Ophthalmology July 1975 JT 00 GANGAF GAPGAF GAN GAP GAP GAN INTERVAL Fig. 6. Cross-correlograms for the three groups of grand average VER's. GAF is the grand average VER to fixed interval stimuli. GAP and GAN are grand average VER's to stimuli synchronized at positive (GAP) and negative (GAN) peaks of the a-rhythm. Ra,a : designates the value of the product-moment correlation coefficient between two averages for a 40 msec. (10 sample points) time interval (represented by one bar in the crosscorrelogram). Time of stimulation is indicated by the black arrow. The averages used to compute the cross-correlograms are shown in the upper right corner of each plot. Scales for the ordinates and abcissae of these are 4.0 MV per division and 100 msec, per division, respectively. by making quantitative comparisons between grand average VER's, and between these averages and their controls using product-moment cross-correlograms. The cross-correlograms between the grand average VER's are shown in Fig. 6. Each bar in the cross -correlogram represents the product-moment correlation coefficient 8 between two grand average VER's calculated over a 40 msec, interval (10 sample points). The cross-correlogram between the grand average VER to stimuli presented at negative a-peaks and that to fixed-interval stimuli (GAN GAF) is shown in the upper portion of Fig. 6. In the 200 msec, interval preceding stimulation, the correlation coefficients oscillate between positive and negative values. The mean correlation coefficient in this interval is These oscillations continue until 120 msec, after stimulation (third bar) at which time there is a positive correlation (0.67) which remains until 400 msec, after stimulation. The mean correlation coefficient in the 120 msec, interval following stimulation is In the interval between 120 msec, and 400 msec, following stimulation, the mean correlation coefficient is The cross-correlogram between the grand average VER to stimuli presented at positive a-peaks, and that to fixed-interval stimuli (GAP* GAF) shown in the middle portion in Fig. 6 behaves in a similar manner. Again, there are oscillations in the 200 msec, prestimulus interval, with a mean correlation coefficient of These continue until 120 msec, after stimulation. The mean correlation coefficient in the 120 msec, interval following stimulation is Notice that in these two intervals, these correlation coefficients are opposite in sign to those in GAN GAF. At 120 msec, following stimulation, there is positive correlation, as in GAN GAF, which remains until 400 msec, following stimulation. In this interval, the mean correlation coefficient is The contrasting values of GAN GAF and GAP* GAF in the 200 msec, interval

7 Volume 14 Number 7 Occipital rhythms and VER 543 preceding stimulation, and the 120 msec, interval following stimulation suggests that the majority of activity in these intervals in GAN and GAP is a-rhythm. They are entirely predictable on the basis of the expected 180 phase difference between GAN and GAP in these intervals. On the other hand, the observation that both cross-correlograms assume positive values after 120 msec, following stimulation indicates the presence of a component which may be independent of the a- rhythm. Similar conclusions are reached by considering the cross-correlogram between the a-synchronized grand average VER's (GAN GAP) shown in the lower portion of Fig. 6. In the 200 msec, interval preceding stimulation, and in the 120 msec, interval following stimulation, the large negative correlation coefficients suggest that this activity is a-rhythm. One hundred-twenty milliseconds following stimulation, however, the cross-correlogram becomes positive, indicating the appearance of the a- independent component. From 200 msec, preceding stimulation, to 120 msec, following stimulation, the mean correlation coefficient is In the interval between 120 msec, and 400 msec, following stimulation, the mean correlation coefficient is The ability of the a-rhythm to mask the early portions of the "ideal VER," as well as the independence of the later components of the VER from the a-rhythm is further demonstrated by the cross-correlograms between each of the a-synchronized grand average VER's and their respective controls shown in Fig. 7. In the cross-correlogram between the grand average VER to stimuli delivered at positive a-peaks and its control grand average (GAP* GAPC), there is a large positive correlation coefficient in the 200 msec, prestimulus interval (mean = 0.97), which continues in the 120 msec, interval following stimulation (mean = 0.66). Corresponding intervals in the cross-correlogram between the grand average VER to stimuli delivered at negative a-peaks and its con- 1.0 CN J? GAPGAPC GAP GAPC GANC INTERVAL Fig. 7. Cross-correlograms between the grand average VER's to negative and positive a-synchronized stimuli (GAN and GAP) and their respective control averages (GANC and GAPC). Averages appear in the upper right corner of each plot. Details are given in Fig. 6. trol grand average (GAN GANC) show similar behavior. In the 200 msec, prestimulus interval the mean correlation coefficient in GAN GANC is In the 120 msec, poststimulus interval, the mean correlation coefficient in GAN GANC is From 120 to 400 msec, after stimulation, both GAP GAPC and GAN GANC have correlation coefficients which oscillate between positive and negative values. The mean correlation coefficient in this interval in GAP GAPC is 0.19 and in GAN GANC is In view of the fact that the correlation coefficients in this interval in GAP GAPC are opposite in sign to those

8 544 Trimble and Potts Investigative Ophthalmology July 1975 in GAN GANC, this oscillatory behavior reflects the absence of a-rhythm in both grand average VER's during this time. Visual inspection of the grand average VER's, as well as comparisons between cross-correlograms suggest that during a- synchronized stimulation, the a-rhythm can completely mask components of the "ideal VER" occurring in the 120 msec, interval following stimulation. Furthermore, they suggest that the portion of the VER between 120 msec, and 400 msec, following stimulation is not obscured by the a- rhythm, and that the latency of this component is not affected by the phase relationships between stimulus and a-rhythm. By presenting a photic stimulus in phase with the a-rhythm, we have, of course, maximized the amount of a which appears in the final average VER, thereby masking its early components. The degree to which such masking would occur during non-asynchronized stimulation would depend on the amount and amplitude of a-rhythm present in the subject's EEG, and the precise phase relationships between the a- rhythm and the stimulus. Complete attenuation of the a-rhythm by averaging techniques would require a uniform random distribution of the stimulus over one cycle of a. The degree to which such uniformity is attained depends, in turn, on the sample size. Reperusal of the control averages taken at fixed intervals shown in Fig. 3, however, demonstrates that the optimum sample size for complete a attenuation may vary from subject to subject. Considering these factors, it may be possible to decrease the effects of a on the early components of the VER by giving stimuli at a time when there is little or no a-rhythm in the EEG. Such a technique would be preferable to simply increasing the sample size since in longer experimental trials, habituation becomes a significant problem. There is, of course, the possibility that the phase relationships between a-rhythm and the stimulus may be deterministic, rather than random. It is well documented that periodic photic stimuli can drive the a-rhythm over a wide frequency range. 9 " 11 If a-driving were operating to the extent that early components of the VER were being masked by synchronized a-rhythm, increasing the sample size for averaging would have little effect on the signal-tonoise ratio. Perhaps the most convincing argument that the a-rhythm is a principal determinant of the signal-to-noise ratio for early components of the VER is that patterned stimuli, which require greater subject vigilance, produce a VER which is less variable between subjects. 12 ' 1M Portions of the VER between 120 msec, and 400 msec, following stimulation, however, are less likely to be masked by the a-rhythm. The most likely explanation for this finding is that the a-rhythm has been blocked during this interval. Since the early animal studies of Bishop, 11 many investigators have shown that the a-rhythm can be temporarily blocked, or desynchronized, by a photic stimulus. During the period in which a is blocked, the signal-to-noise ratio of the VER should be the greatest. Furthermore, components should appear consistently in this period, regardless of the phase relationships between a and the stimulus. This is precisely what we have found. Undoubtedly, this is why Perry and Childers 15 report that most investigators find a major deflection in the VER between 100 and 300 msec, following stimulation. One question remains, however, as to the differences between the grand average VER's to a-synchronized stimulation, and the slight differences we found in the crosscorrelograms between each of the a-synchronized grand average VER's and their respective controls. In view of our findings regarding masking of early VER components by the a-rhythm, we feel that the differences between the grand average VER's to a-synchronized stimulation are produced by a linear, algebraic summation of the VER and the a-rhythm. The differences in the cross-correlograms GAN GANC and GAP CAPC in the 120 msec, interval following stimulation, however,

9 Volume 14 Number 7 Occipital rhythms and VER 545 GAN GANC GAPC GAP + GAN GAPC + GANC GAF GAFC Fig. 8. The results of algebraic summation of the grand average VER's to positive (GAP) and negative (CAN) a-synchronized stimulation (GAP* GAN). The grand average VER to fixedinterval stimulation (GAF) is shown for comparison. The divisions on the ordinates and abcissae of each plot represent 4.0 /*V and 100 msec, respectively. suggest that the degree to which the a- rhythm is blocked by a photic stimulus may be dependent on the phase relationships between stimulus and a-rhythm. Such dependency has been previously suggested by Remond and Lesevre. 7 If this were the case, simple addition of the a-synchronized grand average VER's should show any a which is present in one, but not the other. Fig. 8 shows the results of such an addition. After the peak-to-peak amplitudes of the two averages had been equalized, they were simply algebraically summed. It is clear that there is little difference between this sum and the grand average to fixed interval stimuli (product moment correlation coefficient = ). The degree to which a-rhythm is cancelled by summation is shown in Fig. 9. We feel this is sufficient evidence to suggest that a-blocking is not dependent on the phase of a-synchronized stimulation. Conclusions In conclusion, we have found: (1) That the a-rhythm is capable of completely Fig. 9. The results of algebraic summation of the grand average controls for positive (GAPC) and negative (GANC) a-synchronized stimulation (GAPC + GANC). The grand average control for fixed-interval stimulation (GAFC) is shown for comparison. The divisions on the ordinates and abcissae of each plot represent 4.0 nv and 100 msec, respectively. masking components of the "ideal VER" occurring prior to 120 msec, following stimulation, and that the degree to which such masking occurs during non-a-synchronized stimulation depends on the amount and amplitude of the a-rhythm, and the phase relationships between stimulus and a-rhythm. If these phase relationships are random, the degree of a-attenuation by averaging will depend on sample size, the optimum sample size may differ between subjects. The phase relationships may not be entirely random due to a-driving; (2) that the portion of the VER between 120 msec, and 400 msec, following stimulation is not affected by alpha rhythm due to a-blocking; (3) that the differences between a-synchronized VER's are due to a linear, algebraic summation of VER and a-rhythm; and (4) that the degree to which the a-rhythm is blocked by a photic stimulus does not depend on the phase

10 546 Trimble and Potts Investigative Ophthalmology July 1975 relationships between stimulus and a- rhythm. Of course, these findings relate only to stimuli presented at peaks of the a-rhythm. Currently, we are repeating this study for stimuli delivered at positive and negative slopes of the a-cycle. In conclusion, we feel that recognition of the masking effects of the a-rhythm on the VER is an important first step toward obtaining a more reproducible intersubject VER. This, in turn, is a necessary step in determining the origins of this response and increasing its clinical and experimental value. We wish to thank Dr. Joel Pokorny for his helpful comments during the course of this study. We also wish to thank Mr. Michael Franco who designed and constructed the apparatus for delivering a-synchronized stimuli, and Mr. Gilbert Ng who assisted us in the digital computations. REFERENCES 1. Potts, A. M., and Nagaya, T.: Studies on the visual evoked response. I. The use of the 0.06 red target for evaluation of foveal function, INVEST. OPHTHALMOL. 4: 303, Potts, A. M., and Nagaya, T.: Studies on the visual evoked response. II. The effect of special cortical activity, INVEST. OPHTHAL- MOL. 6: 657, Bechtereva, N. P., and Zontov, Z. Z.: The relationship between certain forms of potentials and the variations in brain excitability, EEC Clin. Neurophysiol. 14: 320, Callaway, E., and Layne, R. S.: Interaction between the visual evoked response and two spontaneous biological rhythms: the EEG alpha cycle and the cardiac arousal cycle, Ann. N. Y. Acad. Sci. 112: 421, Dustman, R. E., and Beck, E. C: Phase of «-waves, reaction time, and visually evoked response, EEG Clin. Neurophysiol. 18: 433, Kooi, K. A., and Bagchi, B. K.: Observations on early components of the visual evoked response and occipital rhythms, EEG Clin. Neurophysiol. 17: 638, Remond, A., and Lesevre, N.: Variations in average visual evoked potential as a function of the a-rhythm phase (autostimulation), EEG Clin. Neurophysiol. (Siippl.) 26: 42, Hays, W. L.: Statistics for Psychologists. New York, 1963, Holt, Rinehart, and Winston. 9. Walter, V. J., and Walter, W. C: The central effects of rhythmic sensory stimulation, EEG Clin. Neurophysiol. 1: 57, Mundy-Castle, A. C: An analysis of central responses to photic stimulation in normal adults, EEG Clin. Neurophysiol. 5: 1, Kitasato, H.: The relation between photic driving of the EEG and the response evoked by photic stimulation in man, Jap. J. Physiol. 16: 238, Trimble, J. L., and Potts, A. M.: Unpublished data. 13. Fatechand, R.: Personal communication. 14. Bishop, G. H.: Cyclic changes in excitability of the optic pathway of the rabbit, Am. J. Physiol. 103: 213, Perry, N. W., and Childers, D. C: The Human Visual Evoked Response: Method and Theory. Springfield, 1969, Charles C Thomas, Publisher.