Peripheral contrast reversal inhibits visually evoked potentials in the fovea

Vision Research Vol. 21. pp. Printed m Great Britain

947 to 950.

1981

@X.2-6989/81/06@?47-04302.00/0 Pergamon Press Ltd

RESEARCH NOTE

PERIPHERAL CONTRAST REVERSAL INHIBITS VISUALLY EVOKED POTE~IALS IN THE FOVEA* ARNE VALBERG, BORGAR T. OLSEN and STEIN MARTHWSEN Institute of Physics, Department of Biophysics, University of Oslo, N-Oslo 3, Norway (Received 16 February 1980)

Abstract-Visual evoked potentials (VEP) to a 0.7” fovea1 test spot of different luminances projected on a white background were recorded with (I) a stationary peripheral black and white grating, and (2) with contrast reversal of the peripheral grating. In the latter case, the near-threshold reduction of visibility of the test spot was accompanied by a reduction of VEP amplitude. To restore threshold visibility or to return to the former amplitude, the same luminance compensation was required. The VEP technique proved to be very sensitive; clear responses were obtained below the visibility threshold, and the response curves showed saturation for a Weber ratio of only 1%.

The threshold visibility of a fovea1 test spot is reduced when the background is suddenly displaced (MacKay, 1970), or when a black and white luminance grating is jerked to and fro by half a cycle in the periphery of the visual field (Breitmeyer and Valberg, 1979; Valberg and Breitmeyer, 1980; Breitmeyer et al., 1980). The latter “jerk effect” is maximal when the test spot is flashed on a background with a luminance close to the space averaged luminance of the peripheral grating, and when the frequency of oscillation is 4 Hz. The reduction of threshoId sensitivity can be rccontiled with the neurophysiolo~~l periphery effect (McIlwain, 1966; Ikeda and Wright, 1972) and shift effect (Kruger and Fischer, 1973; Fischer and Kruger, 1974; Barlow et al., 1977) provided that these excitatory retinal effects manifest themselves as inhibition at a subsequent level of processing (Valberg and Breitmeyer, 1980). Excitatory as well as inhibitory effects have been found in the lateral geniculate nucleus of the cat and monkey (Kruger, 1977). Visual evoked potentials (VEP) to luminance changes and psychophysi~l thr~holds do not always correlate (Regan, 197Oa, 1970b). However, visual thresholds of luminance gratings have been demonstrated to correlate with VEP (Campbell and Maffei, 1970). Since the periphery and shift effects facilitate the near-threshold activity of retinal ganglion cells, one might expect the VEP response to an incremental test spot (flashed on a white background) to be increased by an oscillating peripheral grating. Conversely, from the inhibition hypothesis advocated by Valberg and Breitmeyer (1980), one might expect the VEP amplitude to the flashing test spot to be smalier when the peripheral grating is oscillating than when it * Parts of this paper were presented at the 1. European Meeting on Sensory and Perceptual Processes, Marburg, W-Germany, March 20-22,1978.

is stationary. The following experiment was performed to test this expectation. The VEP-measurements were made with a conventional differential recording technique with one electrode situated 2 cm above the inion and the other on the forehead. The ground electrode was placed on the ear. The cut-off frequencies of the high pass and low pass filters of the preamplifier were 30Hz and 0.1 Hz, respectively. The recordings were made online with a Nord 10 computer programmed for averaging the signals within intervals of 5OOmsec duration. Two observers participated in the experiment. Only observer A.V. had participated in the former psychophysical experiment. The observer was seated 8Ocm away from a black and white TV-monitor. The stimulus pattern generated on the monitor is shown in the insert of Fig. 2. The diagonal of the TV-screen subtended an angle of 33”. The visual angle of the black and white bars of the grating was 0.93” each, corresponding to a spatial frequency of O.%c/deg. The space average luminance, L, of the grating was constant and 20cd*m-*, which was the same as the lwninance of the white background disk. The luminance contrast of the grating was 800?. A background disc of 43”dia made out of white cardboard was mounted on the screen. A test spot of 0.7” dia was superimposed on this background by means of a projector. It was flashed once a second, and the duration of each flash was 1OOmsec. A fixation mark was located near the edge of the test spot securing a fovea1 presentation. Care was taken that the onset of the test flash did not occur in any way synchronous with the contrast reversal of the grating. In this way, the VEP responses generated by the reversing peripheral grating were nulled out by averaging the responses to the test flash. Controls showed that this requirement was always fulfilled. Fifty to 300 947

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Fig. I. The VEP responses to a 1OOmsec fovea1 test flash of increasing luminance, AL, projected on a background disc of luminance L = 20 cd.m-‘. For the same ratios AL/L, the left column “NO PR” (no pattern reversal) shows the responses obtained in the presence of a stationary peripheral luminance grating, and the right column “PR(4Hz)” (pattern reversal) displays those obtained when grating contrast was reversed at a frequency of 4 Hz. Observer A.V. Positivity at inion downwards.

sweeps were averaged depending on the luminance of the test spot. The black and white bars of the grating were either stationary (No PR in Fig. 1) or reversed (PR in Fig. 1) with a frequency of 4 Hz (interchanging position 8 times per set). In either case, and for a condition of strict fixation, the VEP was recorded for different luminances AL of the test spot. The experimental session started with the highest luminance corresponding to a Weber ratio, AL/L, of about lo%, where L is the luminance of the background disc. Each session lasted for about li hr. Plots of the VEPamplitude in PV as a function of log AL/L constitute the desired response curves. In Fig. 1, the responses to light flashes of different luminances are shown when the grating was stationary or its contrast reversed. For the same values of the Weber ratio AL/L, the column “No PR” shows the responses with the stationary grating, and “PR (4Hz)” those obtained with peripheral contrast * The delay of the negative component of 130 msec did not change with the luminance of the test spot as did that of the main positive component. In plotting the two response curves for each observer in Fig. 2, the delay of the measured component (from the onset of the stimulus to the maximum amplitude) in both cases were chosen from the same curve of decreasing delay with increasing luminance (insert). Despite the fact that the delay to the maximum amplitude was dependent on the response in PV rather than on the luminance, the flatness of the positive component at low luminances, lead to pratically the same response curves using either maximal amplitude or the proper delay to determine response magnitude. For observer A.V., measurements for the highest Weber ratios are contaminated by noise, making it difficult to interpret these oversaturated responses. For smaller Weber ratios, however, the variability is low.

modulation. The VEP recorded had a major positive peak at about 2OOmsec which was preceded by a negative peak at about 130msec. Amplitudes were measured peak to peak. Fig. 2 demonstrates the relationship between log AL/L of the test spot and the VEP-amplitude of the main component for the same two stimulus conditions. The dashed and solid curves are fitted to the data points obtained with a stationary and contrastreversing grating, respectively (on two different days). Up to a Weber ratio of lxj Fig. 2 shows a linear relationship between the amplitude and log AL/L. The amplitudes are reduced in the caFe of peripheral contrast reversal. For each observer, ti:: slopes of the response curves for the two experimental situations are equal, being somewhat steeper for T.S. than for A.V. Hence, there is a constant amplitude difference for the whole luminance range up to the point where the responses saturate. Surprisingly, both response curves saturate at a Weber ratio of only 1%. After the responses have reached saturation, the amplitudes obtained with a stationary grating tend to “over saturate”. Only the near-threshold responses are relevant for the comparison with the psychophysical results*. Below saturation, and not only close to the psychophysical threshold, the Weber ratios evoking the same amplitude with and without PR differ by 0.3 log unit for A.V. and by 0.2 log unit for T.S. For observer A.V., the 0.3 log unit difference is close to that found earlier in the psychophysical experiment (Valberg and Breitmeyer, 1980). It should be noted, that the VEP results were obtained with very weak stimuli. The Weber ratios for Soo/, chance of seeing are indicated by the broken lines in Fig. 2. Note that VEP can be

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Fig. 2. The amplitudes of the main component of the VEP for two observers plotted as a function of log AL/L. The dashed curve (open symbols) was obtained with a stationary peripheral grating (no PR), and the fully drawn curve (solid symbols) was obtained with temporal contrast reversal (PR 4 Hz). The upper insert shows the stimulus field. The lower insert displays the dependency of the delay or implicit time (measured from the onset of the test spot to the maximum amplitude of the main component) on the luminance of the test spot. The horizontal and vertical dashed lines indicate the perceptual threshold for the two stimulus conditions. Squares and circles refer to two different days of measurement.

recorded below psychophysical threshold. For the observer T.S., the VEPs under both condition were 2 PV at threshold, while for A.V. they were 4@. About 9 months later, we repeated the experiments on three different days for one observer in order to check this correspondence between the psychophysical and electrophysiological methods. In the psychophysical experiment, the mean difference in the Weber ratios was 0.20 f 0.01 log unit at threshold. The corresponding difference in the Weber ratios between the straight lines obtained by plotting the VEP amplitude as a function of log AL/L, as in Fig. 2, was closely the same (0.21 log unit). The amplitude at the 50% threshold level was 3.5 f 0.3 PV for both experimental conditions (with and without PR). The correspondence tiund earlier was thus confirmed. In all experiments,. surprisingly good VEP responses were obtained for test stimuli that were so far below the Soo/, level as to be invisible to the observer (Fig. I). The experiments were also repeated with 1 and 2 log unit lower luminance of the background disc only. This resulted in somewhat smaller differences between the Weber ratios, AL/L, that gave a constant threshold amplitude (or threshold visibility) for the two stimulus conditions. These experiments correlate well with the reduction of fovea1 threshold visibility of the jerk effect. In the “.R.216 M

psychophysical experiments, a barely visible test spot fell below threshold and- could no longer be seen when the peripheral black and white bars were reversed with a frequency of 4Hz. This was interpreted as long-range lateral inhibition (Valberg and , Breitmeyer, 1980). Similarly, the VEP-amplitude is reduced by contrast reversal for a restricted luminance range below and above the psychophysical threshold. Despite of this, inspection did not reveal a significant perceptual change of brightness of the suprathreshold test spot for the two stimulus conditions. The early saturation at a Weber ratio of 1% may be related to the surprisingly high sensitivity of the VEP for this configuration of light stimulation. Decreasing the luminance of the background disc did not enhance the effect as would be expected if the oscillating grating induces straylight or related neuronal noise in the fovea. In the psychophysical experiment, the magnitude of threshold elevation is maximal when the background disc has a luminance close to the space average luminance of the grating. It decreases for luminance above or below this value. This result also makes it unlikely that the effects are related to attention or cognitive responses to detection. Peripheral contrast reversal or grating oscillations

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to some degree mimic the image displacement that occur with sudden eye movements. Peripheral-transient on foveal-sustained neuron inhibition may constitute a mechanism for this suppression (Breitmeyer and Valberg, 1979). The high sensitivity of the VEP method using a small fovea1 stimulus, points towards new possibilities of application of this technique in vision research, neuroophthalmology and neurology.

,4cknowledgements-The

authors want to thank Professor

D. M. Regan, Professor G. B. Arden, Drs B. Breitmeyer, J. Kruger and L. Spillmann for their critical reading of the manuscript. We also want to express our appreciation to Professor I. Lie at the Institute of Psychology, University of Oslo for placing laboratory facilities at our disposal. REFERENCES

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