0042-6989/91 s3.00 + 0.00 Copyright 0 1991 Pcrgamon Pnss plc
Vision Rcs. Vol. 31. No. 9, pp. 15094516, 1991 Printed in Great Britain. All rights rcscrwd
VISUAL EVOKED POTENTIAL RESPONSES OF THE ANESTHETIZED CAT TO CONTRAST MODULATION OF GRATING PATTERNS X. D.
PANG*and A. B. BONDS
Electrical and Biomedical Engineering, Vanderbilt University, Nashville, TN 37235, U.S.A. (Received 20 Jme
1990; in revised form 21 November 1990)
Abstract--Contrast modulation affords independent control of static contrast (C) and changes in contrast (AC). We found that in anesthetixed, paralyzed cats, the visual evoked potential (VEP) was dependent only on IACI at each pattern transition, and was independent of the starting or ending contrast level. Increasing modulation frequency to above 2Hz reduced the VEP monotonically, implying that the time constant for differentiation by the VEP is of the order of 250 msec. The essentially perfect a.c. coupling suppresses standing contrast completely, permitting the full dynamic range of the VEP response system to be used for detection of contrast increments (which results in a decreasing Weber fraction). The difference between our results and those of behavioral studies using contrast modulation can be explained by eye movements present in the behavioral studies which refresh the retinal image of the static contrast in a way uncorrelated to temporal modulation of the stimulus, thus introducing a masking effect. Contrast modulation
Dynamic contrast response
Visual evoked potential
INTRODUCTION When the contrast level of a visual pattern is temporally modulated by step changes, a brain potential is evoked in the observer. The dependence of this visual evoked potential (VEP) amplitude on the contrast of grating patterns has been reported for both the human (Campbell & Kulikowski, 1972; Bain & Kulikowski, 1976) and the cat (Campbell, Maffei & Piccolino, 1973). When a sinusoidal grating pattern is either flashed on and off from a uniformly illuminated background (On-Off modulation) or spatially phase-reversed, the VEP amplitude is approximately proportional to the logarithm of the contrast. Some behavioral studies have shown that the detection of a threshold change in contrast can be affected by the presence of a steady ambient contrast (Kulikowski & Gorea, 1978; Legge 8t Foley, 1980; Smith, Harweth, Levi & Boltz, 1982). For weaker background contrasts (below about 5%) facilitation is seen, whereas for higher contrasts a masking effect increases threshold. Likewise, in the human VEP the response to a contrast increment is reduced *Current address to which correspondence should be addressed: Research Laboratorv of Electronics. Massachusetts Institute of Technoldgy, Cambridge, MA 02139, U.S.A.
Image stabilization
when the increment is superimposed on a steady contrast above 5% (Bobak, Bodis-Wollner 8~ Marx, 1988). A possible substrate for this behavior is found in single visual cortical cells of the cat, where suprathreshold response amplitude is reduced in the presence of nonzero ambient contrast (e.g. Ohzawa, Sclar & Freeman, 1982). In all of these studies, the ambient contrast that triggered threshold elevation or gain reduction was not truly static. For the behavioral studies, although the pattern itself was stationary, its retinal image was not due to constant eye movement. Stimuli in the single-unit studies were drifting sinusoidal gratings. A primary goal of our study was to examine the dependence of the gain control on dynamic (time-varying) stimuli by assessing the impact of a truly static background contrast (in the absence of eye motion or drift) on suprathreshold responses to changes in contrast. This issue cannot be examined using On-Off or phase-reversal modulation of contrast, since in either case the change in contrast is not independent of the average ambient contrast. Here the contrast of sinusoidal gratings was modulated such that each grating had both a nonzero steady contrast component and a changing contrast component that could be independently manipulated. The VEP responses to step contrast modulation were recorded
1509
1510
X. D. PANG and A. B. E~ONDS
in anesthetized, paralyzed cats. Under these measuring conditions, the VEP response amplitude depended solely on the amount of change-in-contrast and was independent of the background contrast. The temporal characteristics of the VEP response indicate that the system stabilizes within 250 msec of a step change in contrast. The absence of a component of gain control’tider these conditions suggests the existence of .a contrast differentiator that is both rapid and powerful, permitting the allocation of all available dynamic range to the detection of dynamic visual information.
anesthesia (Hammond, 1978). A breathing mixture of nitrous oxide, oxygen and carbon dioxide was delivered at a ratio of 75:23.5: 1.5%. The animal was respired at 30 strokes/min and the stroke volume was adjusted to maintain the peak CO, content in the expiratory air at [email protected]%. Lung pressure was also monitored for indication of adequate gas exchange. Body temperature was maintained at about 37.5”C. Monitoring of brain and heart activity gave indications of the state of anesthesia and physiological conditions. Sinewave gratings were generated digitally on a Joyce Electronics display that could produce patterns with contrast levels of up to 100%. METI$lDS Stimuli were generated in blocks lasting 8 or Experiments were conducted monocularly 10 set and each test condition was presented on 11 eyes in 7 adult cats (2.6-4.0 kg). All in random order to minimize the effects of procedures were carried out under the guidethe intrinsic response variability and to avoid lines of the ARVO Resolution on the Use of systematic adaptation (Bonds, 1984). Each Animals in Research. Anesthesia was induced test condition was presented 20 or 25 times with fluothane and maintained during surgery to achieve a cumulative exposure of 200 sec. with intravenous injection of 2.5% surital A blank presentation of zero contrast was (thiamylal sodium). After insertion of a tracheal included to provide a measure of noise in cannula, the cat was mounted in a stereotaxic the VEP. Contrast changes were always step headholder. The scalp was reflected on the functions in time. Response waveforms were midline and stainless electrodes were implanted digitized with 12 bits of resolution and loaded through the skull onto the dura at bregma into histograms unique to each test condition (indifferent electrode) and at H-C coordinates at 128 bins/set. With a Fourier transform of LO, P4 (recording electrode) which is centered the recorded waveform, the r.m.s. value of between the area centralis representations in the relevant Fourier components (Snyder & Area 17. Evoked potentials were amplified by Shapley, 1979) up to 30 Hz provided a measure 10,000, low-pass filtered at 100 Hz and sent to of the strength of the potential. For example, when a grating is temporally modulated at 1 Hz a computer for further processing. with two transitions (one increase and one The cat’s pupil was dilated with 1% atropine sulfate, and 10% phenylephrine HCl was decrease in contrast) per set, since each transition evokes a potential, the relevant Fourier applied to retract the nictitating membranes. A contact lens with a 4 mm artificial pupil was components are then all the even components [see the middle trace in Fig. 4(B), the response applied to the eye with 3% saline. The refractive waveform in this case is repeated at 2 Hz]. state of each eye was determined by direct Stimuli were stationary sinewave gratings ophthalmoscopy. Spectacle lenses mounted whose contrast level was temporally modulated 1 cm in front of the eye rendered the stimulus image conjugate with the retina. The center of as step functions. The base contrast C and the stimulus field was aligned with the area change-in-contrast AC could be controlled independently. Starting from a base level C,, the centralis of the retina with a reversible ophthalcontrast was first decreased by -(AC) to C2, moscope. The screen was placed 57 cm in front of the eye, and the circular stimulus field sub- then increased by AC back to C,; this process was repeated with a 50% duty cycle. In no case tended an angle of 18 degrees. The spatial mean was AC greater than the base contrast. When luminance of the display was always maintained at 280 cd/m2 (P4 phosphor). The unused eye was the two were equal, this constituted the special case of On-Off modulation. Except where covered. The cats were paralyzed with flaxedil (gal- noted, the gratings had a spatial frequency of lamine triethiodide) at 10 mg/kg hr delivered in 0.4 or 0.5 c/deg, were oriented horizontally and lactated Ringer’s solution containing a small temporally modulated at 1 Hz. Control experiments indicated that these parameters were amount of surital (1 mg/kg hr) to help stabilize
1511
VEP and contrast modulation in cat
Since in our experiments the mean luminance (L,,) was held constant for all contrast levels:
Shaded sres: oA
,
Lmax
-_---------_-
____
- _________.
_ ___
1 C'
L mean=
Lmax + Lmi~ = L6ax
+ Lki~
(3)
2
2
the difference in contrasts: -JL)+(Lli,-GliIl) 2(L )
AC=CLCJLL
mcsn
._
=
L’max -L, _
*
(4)
___
The last equality results from the fact that for symmetrical gratings L&, - L_ = Ltin - LA,, . RESULTS
Fig. 1. Contrast modulation of a sinewave grating. L denotes absolute luminance, C contrast. Shaded area shows the amount of luminance redistributed during a modulation cycle.
most effective for evoking maximum VEP responses in the ranges of 0.2-l .6 c/deg for spatial frequency (Pang, 1983; Bonds, 1984), O-135 deg for orientation, and 0.54 Hz for temporal frequency (see also Fig. 4). The contrast C is defined as (see Fig. 1):
- Lmin c= Lmax
Lm, + &in
where L,,,, and Lmi, are the maximum and minimum luminance, respectively. The contrast level was modulated by adding a contrast change AC: L’ - Ld” mLx Lb,+ L&“’
C+AC=C’=
(2)
Base Contrast C (%I 100
A plot of the VEP response amplitude vs the change-in-contrast AC parametric on the base contrast C (Fig. 2A) shows that response amplitude was approximately proportional to log JAC I. However, no systematic dependence is seen on the base contrast C. This is emphasized in Fig. 2B, which replots similar data from another cat and shows that the VEP amplitude was flat as base contrast C assumed values from 34% to 100%. Figure 3 confirms this result with data pooled from 4 animals and averaged, for C ranging from 16 to 96% and 1AC 1 from 8 to 76%. The effective stimulus for the VEP is thus solely the change-in-contrast; response amplitude is independent of the absolute contrast at either extreme. Figure 3A, which has a logarithmic horizontal scale, also shows that the response amplitude was on the whole proportional to the logarithm of IACI. This is not unexpected since the a-34 ‘~-23 A-15 o-10
(4
o-62 o-40 a-34
_ _ _ - - - - _ _ _ - N”,,
5
IACI (%I @)
loo-
00 # 30 P 3 40 _m d 20,
Primary results
11
14 IACI (%I
10
25
[
00.
g
60,
f
40,,
8
20
x * -_-_34
----__ 50
&,, 76
100
Base Contrast C (%)
Fig. 2. (A) VEP response amplitude (in percentage of the maximum) vs (AC 1x 100% at different base contrasts from a single measurement series. The “null” line indicates noise level (PV3:A3.19). All horizontal axes in the figures of this paper are logarithmic except for Figs 1 and 4B. (B) VEP amplitude vs base contrast, parametric on IAC 1, from one measurement series (PV4:A1.08).
1512
X. D. PANGand A. B. BONDS
loo% % g
I
l&cl 6)
80-
.-
76
60-
tr x-
g 32
A+o-
24 16 6
-
it B u _: %
Null _
~-~---------------~--
2
03
40-
20
L
OJ
20
10
60
40
1
too
Base Contrast C (a)
Fig. 3. (A) Same as Fig. 2A except that the data shown are a normalized average from 4 animals (PV2, 3, 4 and 5). (B) Same as Fig. 2B except that the data shown are a normalized average from 4 animals (PV2, 3, 4 and 5).
ON-OFF
Contrast
(%) Temporal Frequency
(Hz)
v-76
O-23 o-15 B-10
O-50 r-34
O-4 o-2 v-1
(-4)
o-o.5 loo-
100 -
80
80 .’
60
60..
40
.
20 .’
I
, 0.5
1 Temporal
4
2 Frequency
(HZ)
10
15
23 ON-OFF
34
50
76
ContWiSt (%I
SCalC
I
.+._
(B) &/___. -L-_-cc
2.oHz
OSHZ
Null
Fig. 4. (A) The effect of temporal modulation frequency on VEP amplitude. On-Off stimulation (PV4:AlM). (B) The effect of temporal modulation frequency on VEP waveforms. IAC( = 19%, 50% duty cycle On-Off stimulation. Duration of the histogram shown = 1 sec. From the left, odd numbered waves correspond to a decrease in contrast (a negative step change), even numbered waves correspond to an increase in contrast. Note that the response does not depend on the sign of AC. Scale = 30 PV (PV3:A3.10). (C) The effect of temporal modulation frequency on gain (slope) and threshold of the VEP response function. On-Off stimulation (PV4:Al.O4).
1513
VEP and contrast modulation in cat
On-Off and phase-reversing stimuli used in the earlier experiments (Campbell & Kulikowski, 1972; Campbell et al., 1973) were special cases of contrast modulation. This logarithmic relationship, including both the slopes and the extrapolated intercepts of the response regression lines with the noise level, was not affected by the base contrast. With a stabilized background grating, we thus did not find in the cat masking of the VEP response by background contrast such as that found in the behaving monkey (Smith et al., 1982) and human (Kulikowski 8c Gorea, 1978; Legge & Foley, 1980) and the human VEP (Bobak et al., 1988). The above results were obtained from 97 measurement series in 11 eyes (7 cats). The average VEP response peaked at about 2OpV, with a signal-to-noise ratio in the range of 5-10: 1 (after averaging). In 8 cases out of 97, a slightly larger response amplitude was observed with a higher base contrast; in 6 cases, the response amplitude became slightly smaller as the base contrast was increased. Temporal properties of the VEP response
Changes in contrast are clearly the effective stimulus for the VEP, as opposed to steady contrast components. This differentiation mechanism implies that the impact of a contrast step dissipates fairly rapidly. We examined the rate of decay of the perturbation of the system by a step change by varying the temporal frequency of step presentations. Response amplitude was largest and constant for frequencies of 1 Hz and below, but decreased monotonically at 2 Hz and higher (Fig. 4A). Unlike continuous sinusoidal temporal modulation, each contrast step can be thought of as a distinct event. The flatness of the curve at low temporal frequencies implies that there is a minimum temporal separability, here about 250 msec, beyond which each transition (and its subsequent disturbance of the system) may be treated as independent events. Encroachments of a transition into the trailing edge of the response to a previous transition as a result of stimulus frequencies of 4 Hz or greater resulted in marked reduction of the response, as illustrated by the VEP waveforms shown in Fig. 4B. This suggests that in the cat VEP the adaptive impact of any transition is transient, with a duration on the order of 250 msec. The marked .attenuation of the VEP amplitude with temporal frequency also addresses the
issue of the origin of the VEP. Slow potentials such as the VEP are thought to arise primarily from post-synaptic-potential activity in the dendritic arborizations (e.g. Nunez, 1981). The extent to which the VEP reflects cortical activity, as opposed to signals from the lateral geniculate nucleus fibers of projection, remains unknown. In the cat, most retinal ganglion cells and geniculate cells have a broad temporal bandpass, often responding to Bicker in excess of 304OHz (e.g. Enroth-Cugell & Shapley, 1973). Cells in the cat visual cortex are by comparison sluggish, with the temporal cutoff frequency usually being limited to about 3-10 Hz (Movshon, Thompson & Tolhurst, 1978). The similarly sluggish bandpass seen in the VEP suggests that under our recording conditions it was primarily generated at cortical and/or more central levels. Because of the severe attenuation of the cat VEP at higher temporal frequencies, the use of frequencies beyond 2 Hz to study the cat VEP (e.g. Campbell et al., 1973) clearly deserves reconsideration. The effect of temporal modulation frequency on the relationship between VEP amplitude and log IAC 1 is shown in Fig. 4C. Higher temporal frequencies resulted in a reduced slope on this semilog scale, but the logarithmic nature of the stimulus-response relationship was not changed. Accompanying the reduction in the slope, an elevation of response threshold (intercept of the response line with the noise level) can also be seen. The reduction in response amplitude with temporal frequency is thus a result of a combination of reduced gain and elevated threshold. DISCUSSION
Static vs dynamic contrast The VEP responds solely to pattern transitions rather than static patterns. In our experiments, the cats were paralyzed and the eye movements suppressed. Once the presence of a base contrast was established, the static pattern would not itself generate a VEP response. Our interest was in whether the presence of a static base contrast modifies the VEP response to contrast increments, and our data suggest that is not the case. The VEP response system completely suppressed the standing contrast in favor of differential changes in contrast. If the eye movements were not controlled, however, a static contrast would become “dynamic” on the retina, and therefore could influence (or mask)
1514
X. D.
PANG
and A. B. BONDS
the VEP response to modulated contrast increments. This point is clarified by comparing our results with those from contrast modulation presented to alert subjects. Bodis-Wollner, Hendley and Kulikowski (1972) related VEP response to contrast modulation in the human, and found a dependence of the threshold for contrast modulation on base contrast. Since they were examining the threshold for detecting a change in contrast rather than the suprathreshold stimulusresponse relationship, we derived a threshold from our data for comparison. The justdetectable change-in-contrast, AC,, , is defined by the intercept of a linear extrapolation of the suprathreshold response with the noise level. Figure 3A shows that in the cat VEP, AC,, is essentially independent of base contrast. Since in behaving subjects the retinal image of a static contrast is really “dynamic”, it is not surprising that the mean contrast has an effect on contrastmodulation threshold. We feel, however, that their interpretation of the direction of the effect is open to question. They concluded that the contrast modulation threshold (which is not AC,,,; see below) decreases (or the “sensitivity” increases) monotonically as a function of the mean contrast, which was defined as the arithmetic mean of the contrasts before and after a grating transition. (Here we equate base contrast in our study with their mean contrast, since at threshold the difference is vanishingly small). In their study, a contrast modulation depth M was defined as M = AC/C_,, and the VEP contrast-modulation threshold Mth was defined as the intercept with zero voltage of the response amplitude as a function of M on a semilog scale. They plotted Mthvs C,,.,,,on a log-log scale and fitted a straight regression line, which had a negative slope, to the data. Such a relationship would mean a reduction in the modulation threshold (or an increase in “sensitivity”) as the mean contrast was increased. If their data are examined from the standpoint of AC,, rather than M,,,, however, a power law dependence of AC,, on C,,, with a positive exponent of about 0.85 emerges, meaning that AC,,, rises (or the sensitivity decreases) as C,,,,, rises. A subsequent study by the same group (Bobak et al., 1988) reaches a conclusion that is more compatible with the contrast masking data (for comparable background contrast) in the human (Kulikowski & Gorea, 1978; Legge & Foley, 1980) and behaving monkey (Smith et al.,
1982). Bobak et al. found that the suprathreshold slope of both the first and second harmonic frequency components of the VEP response became increasingly shallow with higher levels of mean contrast. Since the response level for the two components changed differently with mean contrast, they concluded that the effect was not due to fatigue or response suppression but rather to some form of contrast gain control. A positive dependence of threshold (or negative dependence of slope) on background level is analogous to masking of a tone by noise in the auditory system, since the refreshing of base contrast by eye movement is uncorrelated with contrast modulation. The higher the base or mean contrast, the stronger the “masking” effect. This explanation is also consistent with reports that the slope of the contrast masking function in behaving subjects is smaller for gratings with lower spatial frequencies (Kulikowski & Gorea, 1978; Smith et al., 1982) because gratings with lower spatial frequencies have lower slopes of luminance change and are thus likely to be less effectively refreshed by eye movement. Two issues that frequently rise in comparing results from anesthetized animals with that from awake humans are the use of anesthesia and difference in spatial resolution. It has been reported that when barbiturate doses several times higher than those involved in our study were used, contrast-mediated VEP response could be eliminated (but not altered) in the monkey (Padmos, Haaijman & Spekreijse, 1973; Van der Marel, Dagnelie & Spekreijse, 1981). Since we have always found a reliable and consistent VEP response to pattern transitions under our recording conditions [see Fig. 4(B)] and since our preparations yielded absolute contrast sensitivities comparable to those of the behaving cat (Berkley, 1990) we do not feel that our use of the anesthesia significantly compromised our results. It is known that the spatial frequency corresponding to the peak of contrast sensitivity for the cat is lower than that for the human by a factor of about 10 (Campbell et ,al., 1973). We selected spatial frequencies of 0.4 and 0.5 c/deg, which we found to be most effective for evoking maximum VEP responses in the range of 0.2-1.6 c/deg (Pang, 1983; Bonds, 1984), and which are lower than those used by Bodis-Wollner et al. (1972) and Bobak et al. (1988) in the human by a factor of about 10.
1515
VEP and contrast modulation in cat
Correlations with single-cell studies Ohzawa et al. (1982) reported a contrast adaptation mechanism in cat cortical cells. Elevation of the average contrast during an extended presentation (40 set) of a drifting grating reduced the cell’s response to gratings with different contrasts but otherwise identical to the background grating. This manifestation of gain control would imply a conflict with our failure to find one. However, stimulation conditions differed between the two experiments in two important aspects. First, for the single unit study, the adapting grating was constantly in motion, whereas for this VEP study the background contrast was static. Second, measurements reported here were not preceeded by a prolonged, effective, and constant stimulus, as in the single-unit study. After 30 set of contrast modulation at 1 Hz, we did, however, observe a reduction in the VEP response to contrast modulation of gratings which were identical to the adapting grating except for the level of the background contrast and change-in-contrast (Pang, 1983). The amount of reduction increased with the change-in-contrast of the adapting grating. The logarithmic stimulusresponse relationship was, like in the case of increasing temporal modulation frequency, retained. The adaptation was specific to the spatial frequency and orientation of the grating, with a recovery time of l-2 min. Similar results have been reported by Bonds (1984). This similarity in adaptability to prolonged stimuli between the VEP and cortical cell responses supports the notion that the VEP we recorded was generated at cortical or higher levels. Temporal effectiveness of contrast differentiation In the cat VEP the duration of the impact of any change in contrast was no longer than about 250 msec. After this period, even though contrast might remain, it had little impact on subsequent responses. While complete extinction of the effects of a background grating is not expected in psychophysical experiments due to eye motion, Wilson (1990) has reported a similar onset time course in contrast masking experiments. A 3 c/deg test pattern was superimposed on a similar mask at different onset asynchronies. Test pattern thresholds were elevated by a factor of 10 at 0 msec, but only by 4 after 200 msec. At onset the test threshold was a power function of masking contrast with an exponent of 0.69, whereas after 200msec the
exponent was reduced to 0.39. These observations are consistent with the idea that the impact of a mask dissipates over a period of no more than a few hundred milliseconds, with the exception that some masking component remains in the psychophysical domain, most probably as a result of motion of the retinal image. Functional signiJcance of the AC-VEP ship
relation-
In the experiments described here, the response as a function of change-in-contrast was independent of ambient contrast. Besides the factors discussed previously, an analysis of Fig. 1 may help to elaborate this point. The area of the shaded region in Fig. 1, i.e. the net change in light energy distribution over one spatial cycle resulting from a change in contrast, is: AA=2
‘(L;, s0
- L_)sin(x)
dx
= 4(AC)(L,,)
(9
which depends only on the change-in-contrast AC and the mean luminance [equation (4) is used in the calculation]. Thus, for a given AC, the amount of change in light energy distribution upon a contrast transition is independent on the base contrast C. The AC evoked response system may therefore be considered as a detector of changes in light energy distribution with essentially perfect a.c. coupling (i.e. responses are totally phasic). The consequences of a.c. coupling may be viewed in two ways: the response amplitude resulting from a change in contrast from, e.g. 30-40%, is identical to the amplitude resulting from an On-Off modulation of 10%. Acknowledging the logarithmic stimulus-response function, this is much larger than the difference between the response amplitudes resulting from a 30% and 40% On-Off modulation, respectively. A tendency to suppress static base contrasts thus enhances detection of small changes of suprathreshold contrast, but at the expense of the loss of information on absolute contrast levels. Alternatively, since the response to change-incontrast is independent of the base contrast, the a.c. coupling is not analogous to a Weber’s law mechanism. If threshold, or a just-detectable contrast modulation corresponds to a small, constant response amplitude, then it remains unchanged for all base contrasts. Thus in the contrast domain the Weber fraction (A&/C)
1516
X. D. PANGand A. B.
actually drops as the background contrast increases. A mechanism for the control of contrast gain is required because of the limited dynamic range of the visual cortex. One way of compensation is a nonlinear mapping of contrast to response, here evident in the logarithmic form of the relationship. Were this relationship to remain static, discrimination of different contrasts at or near threshold would be adequate, but discernible contrast increments would rise dramatically as background contrast rose. In cortical single units, a form of contrast gain control is evident from the rightward shift of the contrast-response function as contrast is increased, which keeps the log-linear portion of the response curve centered on the ambient contrast (Ohzawa et al., 1982). The a.c. differentiation found in the VEP performs essentially the same service, effectively resetting the operating point of the system back to zero (where increment sensitivity is high) despite the presence of a standing contrast. The effectiveness of this differentiation is illustrated by the absence of saturation in Fig. 3A. When a standing contrast also becomes “dynamic” on the retina as in behavioral studies, the resetting of the operating point will then not be perfect, as indicated by the reduced slope and saturation seen in suprathreshold VEP responses of human subjects exposed to increasing background contrasts (Bobak et al., 1988). Acknowledgemenf+-We thank Dr E. J. DeBruyn for his aid in animal preparations and Dr R. M. Held of MIT for commenting on an earlier version of the manuscript. A portion of this work was submitted by X. D. Pang as a master’s thesis to the Department of Electrical and Biomedical Engineering, Vanderbilt University, July 1983. This work was supported by the NIH grant EY03778-02 and the Vanderbilt University Research Council. Flaxedil was kindly provided by American Cyanamid.
REFERENCES
BONDS
Bobak, P., Bodis-Wollner, I. & Marx, M. (1988). Cortical contrast gain control in human spatial vision. Journal of Physiology,
London, 405, 421-437.
Bodis-Wollner, I., Hendley, C. D. & Kulikowski, J. J. (1972). Electrophysiological and psychophysical responses to modulation of contrast of a grating pattern. Perception,
I, 341-349.
Bonds, A. B. (1984). Spatial adaptation of the cortical visual evoked potential of the cat. Investigative Ophthalmology and Visual Science, 25, 640-646.
Campbell, evoked pattern. Campbell, contrast
F. W. & Kulikowski, J. J. (1972). The visual potential as a function of contrast of a grating Journal of Physiology,
ology, London, 233, 271-309.
Hammond, P. (1978). On the use of nitrous oxide/oxygen mixtures for anaesthesia in cats. Journal of Physiology, London, 275, 64.
Kulikowski, J. J. & Gorea, A. (1978). Complete adaptation to patterned stimuli: A necessary and sufficient condition to Weber’s law for contrast. Vision Research, 18, 1223-1227. Legge, G. E. & Foley, J. M. (1980). Contrast masking in human vision. JOWMI of the Optical Society of America, 70(12), 1458-1471.
Movshon, J. A., Thompson, I. D. & Tolhurst, D. J. (1978). Spatial and temporal sensitivity of neurons in area 17 and 18 of the cat’s visual cortex. Journal of Physiology, London, 283, 101-120.
Nunez, P. L. (1981). Electric fields of the brain. New York: Oxford University Press. Ohzawa, I., Sclar, G. & Freeman, R. D. (1982). Contrast gain control in the cat visual cortex. Nature, London, 298, 266268.
Padmos, P., Haaijman, J. J. & Spekreijse, H. (1973). Visually evoked cortical potentials to patterned stimuli in monkey and man. Electroencephalography and Clinical Neurophysiology 35, 153-166. Pang, X. D. (1983). Differential contrast gain control in the cat visual cortex. M.S. thesis, Department of Electrical and Biomedical Engineering, Vanderbilt University, Nashville, Tenn. Smith, E. L., Harweth, R. S., Levi, D. M. & Boltz, R. L. (1982). Contrast increment thresholds of rhesus monkeys. Vision Research, 22, 1153-I 161. Snyder, A. & Shapley, R. M. (1979). Deficits in the visual evoked potentials of cats as a result of visual deprivation. Experimental
Bain, R. & Kulikowski, J. J. (1976). Contrast thresholds for pattern and movement detection evaluated by evoked potentials. Journal of Physiology, London. 259, 3435. Berkley, M. A. (1990). Behavioral determination of the spatial selectivity of contrast adaptation in cats: Some evidence for a common plan in the mammalian visual system. Visual Neuroscience, 4, 413-426.
London, 222, 345-356.
F. W., Maffei, I. & Piccolino, M. (1973). The sensitivity of the cat. Journal of Physiology, London, 229, 7 19-73 1. Enroth-Cugell, C. & Shapley, R. M. (1973). Adaptation and dynamics of cat retinal ganglion cells. Journal of Physi-
Brain Research,
37, 73-86.
Van der Marel, H., Dagnelie, G. & Spekreijse, H. (1981). Pattern evoked potentials in awake rhesus monkeys. Investigative 457-466.
Ophthalmology
and
Visual
Science.
21.
Wilson, H. R. (1990). Psychophysics of contrast gain control. Investigative Ophthalmology and Visual Science (Suppl.),
31, 430.
Vision Rcs. Vol. 31. No. 9, pp. 15094516, 1991 Printed in Great Britain. All rights rcscrwd
VISUAL EVOKED POTENTIAL RESPONSES OF THE ANESTHETIZED CAT TO CONTRAST MODULATION OF GRATING PATTERNS X. D.
PANG*and A. B. BONDS
Electrical and Biomedical Engineering, Vanderbilt University, Nashville, TN 37235, U.S.A. (Received 20 Jme
1990; in revised form 21 November 1990)
Abstract--Contrast modulation affords independent control of static contrast (C) and changes in contrast (AC). We found that in anesthetixed, paralyzed cats, the visual evoked potential (VEP) was dependent only on IACI at each pattern transition, and was independent of the starting or ending contrast level. Increasing modulation frequency to above 2Hz reduced the VEP monotonically, implying that the time constant for differentiation by the VEP is of the order of 250 msec. The essentially perfect a.c. coupling suppresses standing contrast completely, permitting the full dynamic range of the VEP response system to be used for detection of contrast increments (which results in a decreasing Weber fraction). The difference between our results and those of behavioral studies using contrast modulation can be explained by eye movements present in the behavioral studies which refresh the retinal image of the static contrast in a way uncorrelated to temporal modulation of the stimulus, thus introducing a masking effect. Contrast modulation
Dynamic contrast response
Visual evoked potential
INTRODUCTION When the contrast level of a visual pattern is temporally modulated by step changes, a brain potential is evoked in the observer. The dependence of this visual evoked potential (VEP) amplitude on the contrast of grating patterns has been reported for both the human (Campbell & Kulikowski, 1972; Bain & Kulikowski, 1976) and the cat (Campbell, Maffei & Piccolino, 1973). When a sinusoidal grating pattern is either flashed on and off from a uniformly illuminated background (On-Off modulation) or spatially phase-reversed, the VEP amplitude is approximately proportional to the logarithm of the contrast. Some behavioral studies have shown that the detection of a threshold change in contrast can be affected by the presence of a steady ambient contrast (Kulikowski & Gorea, 1978; Legge 8t Foley, 1980; Smith, Harweth, Levi & Boltz, 1982). For weaker background contrasts (below about 5%) facilitation is seen, whereas for higher contrasts a masking effect increases threshold. Likewise, in the human VEP the response to a contrast increment is reduced *Current address to which correspondence should be addressed: Research Laboratorv of Electronics. Massachusetts Institute of Technoldgy, Cambridge, MA 02139, U.S.A.
Image stabilization
when the increment is superimposed on a steady contrast above 5% (Bobak, Bodis-Wollner 8~ Marx, 1988). A possible substrate for this behavior is found in single visual cortical cells of the cat, where suprathreshold response amplitude is reduced in the presence of nonzero ambient contrast (e.g. Ohzawa, Sclar & Freeman, 1982). In all of these studies, the ambient contrast that triggered threshold elevation or gain reduction was not truly static. For the behavioral studies, although the pattern itself was stationary, its retinal image was not due to constant eye movement. Stimuli in the single-unit studies were drifting sinusoidal gratings. A primary goal of our study was to examine the dependence of the gain control on dynamic (time-varying) stimuli by assessing the impact of a truly static background contrast (in the absence of eye motion or drift) on suprathreshold responses to changes in contrast. This issue cannot be examined using On-Off or phase-reversal modulation of contrast, since in either case the change in contrast is not independent of the average ambient contrast. Here the contrast of sinusoidal gratings was modulated such that each grating had both a nonzero steady contrast component and a changing contrast component that could be independently manipulated. The VEP responses to step contrast modulation were recorded
1509
1510
X. D. PANG and A. B. E~ONDS
in anesthetized, paralyzed cats. Under these measuring conditions, the VEP response amplitude depended solely on the amount of change-in-contrast and was independent of the background contrast. The temporal characteristics of the VEP response indicate that the system stabilizes within 250 msec of a step change in contrast. The absence of a component of gain control’tider these conditions suggests the existence of .a contrast differentiator that is both rapid and powerful, permitting the allocation of all available dynamic range to the detection of dynamic visual information.
anesthesia (Hammond, 1978). A breathing mixture of nitrous oxide, oxygen and carbon dioxide was delivered at a ratio of 75:23.5: 1.5%. The animal was respired at 30 strokes/min and the stroke volume was adjusted to maintain the peak CO, content in the expiratory air at [email protected]%. Lung pressure was also monitored for indication of adequate gas exchange. Body temperature was maintained at about 37.5”C. Monitoring of brain and heart activity gave indications of the state of anesthesia and physiological conditions. Sinewave gratings were generated digitally on a Joyce Electronics display that could produce patterns with contrast levels of up to 100%. METI$lDS Stimuli were generated in blocks lasting 8 or Experiments were conducted monocularly 10 set and each test condition was presented on 11 eyes in 7 adult cats (2.6-4.0 kg). All in random order to minimize the effects of procedures were carried out under the guidethe intrinsic response variability and to avoid lines of the ARVO Resolution on the Use of systematic adaptation (Bonds, 1984). Each Animals in Research. Anesthesia was induced test condition was presented 20 or 25 times with fluothane and maintained during surgery to achieve a cumulative exposure of 200 sec. with intravenous injection of 2.5% surital A blank presentation of zero contrast was (thiamylal sodium). After insertion of a tracheal included to provide a measure of noise in cannula, the cat was mounted in a stereotaxic the VEP. Contrast changes were always step headholder. The scalp was reflected on the functions in time. Response waveforms were midline and stainless electrodes were implanted digitized with 12 bits of resolution and loaded through the skull onto the dura at bregma into histograms unique to each test condition (indifferent electrode) and at H-C coordinates at 128 bins/set. With a Fourier transform of LO, P4 (recording electrode) which is centered the recorded waveform, the r.m.s. value of between the area centralis representations in the relevant Fourier components (Snyder & Area 17. Evoked potentials were amplified by Shapley, 1979) up to 30 Hz provided a measure 10,000, low-pass filtered at 100 Hz and sent to of the strength of the potential. For example, when a grating is temporally modulated at 1 Hz a computer for further processing. with two transitions (one increase and one The cat’s pupil was dilated with 1% atropine sulfate, and 10% phenylephrine HCl was decrease in contrast) per set, since each transition evokes a potential, the relevant Fourier applied to retract the nictitating membranes. A contact lens with a 4 mm artificial pupil was components are then all the even components [see the middle trace in Fig. 4(B), the response applied to the eye with 3% saline. The refractive waveform in this case is repeated at 2 Hz]. state of each eye was determined by direct Stimuli were stationary sinewave gratings ophthalmoscopy. Spectacle lenses mounted whose contrast level was temporally modulated 1 cm in front of the eye rendered the stimulus image conjugate with the retina. The center of as step functions. The base contrast C and the stimulus field was aligned with the area change-in-contrast AC could be controlled independently. Starting from a base level C,, the centralis of the retina with a reversible ophthalcontrast was first decreased by -(AC) to C2, moscope. The screen was placed 57 cm in front of the eye, and the circular stimulus field sub- then increased by AC back to C,; this process was repeated with a 50% duty cycle. In no case tended an angle of 18 degrees. The spatial mean was AC greater than the base contrast. When luminance of the display was always maintained at 280 cd/m2 (P4 phosphor). The unused eye was the two were equal, this constituted the special case of On-Off modulation. Except where covered. The cats were paralyzed with flaxedil (gal- noted, the gratings had a spatial frequency of lamine triethiodide) at 10 mg/kg hr delivered in 0.4 or 0.5 c/deg, were oriented horizontally and lactated Ringer’s solution containing a small temporally modulated at 1 Hz. Control experiments indicated that these parameters were amount of surital (1 mg/kg hr) to help stabilize
1511
VEP and contrast modulation in cat
Since in our experiments the mean luminance (L,,) was held constant for all contrast levels:
Shaded sres: oA
,
Lmax
-_---------_-
____
- _________.
_ ___
1 C'
L mean=
Lmax + Lmi~ = L6ax
+ Lki~
(3)
2
2
the difference in contrasts: -JL)+(Lli,-GliIl) 2(L )
AC=CLCJLL
mcsn
._
=
L’max -L, _
*
(4)
___
The last equality results from the fact that for symmetrical gratings L&, - L_ = Ltin - LA,, . RESULTS
Fig. 1. Contrast modulation of a sinewave grating. L denotes absolute luminance, C contrast. Shaded area shows the amount of luminance redistributed during a modulation cycle.
most effective for evoking maximum VEP responses in the ranges of 0.2-l .6 c/deg for spatial frequency (Pang, 1983; Bonds, 1984), O-135 deg for orientation, and 0.54 Hz for temporal frequency (see also Fig. 4). The contrast C is defined as (see Fig. 1):
- Lmin c= Lmax
Lm, + &in
where L,,,, and Lmi, are the maximum and minimum luminance, respectively. The contrast level was modulated by adding a contrast change AC: L’ - Ld” mLx Lb,+ L&“’
C+AC=C’=
(2)
Base Contrast C (%I 100
A plot of the VEP response amplitude vs the change-in-contrast AC parametric on the base contrast C (Fig. 2A) shows that response amplitude was approximately proportional to log JAC I. However, no systematic dependence is seen on the base contrast C. This is emphasized in Fig. 2B, which replots similar data from another cat and shows that the VEP amplitude was flat as base contrast C assumed values from 34% to 100%. Figure 3 confirms this result with data pooled from 4 animals and averaged, for C ranging from 16 to 96% and 1AC 1 from 8 to 76%. The effective stimulus for the VEP is thus solely the change-in-contrast; response amplitude is independent of the absolute contrast at either extreme. Figure 3A, which has a logarithmic horizontal scale, also shows that the response amplitude was on the whole proportional to the logarithm of IACI. This is not unexpected since the a-34 ‘~-23 A-15 o-10
(4
o-62 o-40 a-34
_ _ _ - - - - _ _ _ - N”,,
5
IACI (%I @)
loo-
00 # 30 P 3 40 _m d 20,
Primary results
11
14 IACI (%I
10
25
[
00.
g
60,
f
40,,
8
20
x * -_-_34
----__ 50
&,, 76
100
Base Contrast C (%)
Fig. 2. (A) VEP response amplitude (in percentage of the maximum) vs (AC 1x 100% at different base contrasts from a single measurement series. The “null” line indicates noise level (PV3:A3.19). All horizontal axes in the figures of this paper are logarithmic except for Figs 1 and 4B. (B) VEP amplitude vs base contrast, parametric on IAC 1, from one measurement series (PV4:A1.08).
1512
X. D. PANGand A. B. BONDS
loo% % g
I
l&cl 6)
80-
.-
76
60-
tr x-
g 32
A+o-
24 16 6
-
it B u _: %
Null _
~-~---------------~--
2
03
40-
20
L
OJ
20
10
60
40
1
too
Base Contrast C (a)
Fig. 3. (A) Same as Fig. 2A except that the data shown are a normalized average from 4 animals (PV2, 3, 4 and 5). (B) Same as Fig. 2B except that the data shown are a normalized average from 4 animals (PV2, 3, 4 and 5).
ON-OFF
Contrast
(%) Temporal Frequency
(Hz)
v-76
O-23 o-15 B-10
O-50 r-34
O-4 o-2 v-1
(-4)
o-o.5 loo-
100 -
80
80 .’
60
60..
40
.
20 .’
I
, 0.5
1 Temporal
4
2 Frequency
(HZ)
10
15
23 ON-OFF
34
50
76
ContWiSt (%I
SCalC
I
.+._
(B) &/___. -L-_-cc
2.oHz
OSHZ
Null
Fig. 4. (A) The effect of temporal modulation frequency on VEP amplitude. On-Off stimulation (PV4:AlM). (B) The effect of temporal modulation frequency on VEP waveforms. IAC( = 19%, 50% duty cycle On-Off stimulation. Duration of the histogram shown = 1 sec. From the left, odd numbered waves correspond to a decrease in contrast (a negative step change), even numbered waves correspond to an increase in contrast. Note that the response does not depend on the sign of AC. Scale = 30 PV (PV3:A3.10). (C) The effect of temporal modulation frequency on gain (slope) and threshold of the VEP response function. On-Off stimulation (PV4:Al.O4).
1513
VEP and contrast modulation in cat
On-Off and phase-reversing stimuli used in the earlier experiments (Campbell & Kulikowski, 1972; Campbell et al., 1973) were special cases of contrast modulation. This logarithmic relationship, including both the slopes and the extrapolated intercepts of the response regression lines with the noise level, was not affected by the base contrast. With a stabilized background grating, we thus did not find in the cat masking of the VEP response by background contrast such as that found in the behaving monkey (Smith et al., 1982) and human (Kulikowski 8c Gorea, 1978; Legge & Foley, 1980) and the human VEP (Bobak et al., 1988). The above results were obtained from 97 measurement series in 11 eyes (7 cats). The average VEP response peaked at about 2OpV, with a signal-to-noise ratio in the range of 5-10: 1 (after averaging). In 8 cases out of 97, a slightly larger response amplitude was observed with a higher base contrast; in 6 cases, the response amplitude became slightly smaller as the base contrast was increased. Temporal properties of the VEP response
Changes in contrast are clearly the effective stimulus for the VEP, as opposed to steady contrast components. This differentiation mechanism implies that the impact of a contrast step dissipates fairly rapidly. We examined the rate of decay of the perturbation of the system by a step change by varying the temporal frequency of step presentations. Response amplitude was largest and constant for frequencies of 1 Hz and below, but decreased monotonically at 2 Hz and higher (Fig. 4A). Unlike continuous sinusoidal temporal modulation, each contrast step can be thought of as a distinct event. The flatness of the curve at low temporal frequencies implies that there is a minimum temporal separability, here about 250 msec, beyond which each transition (and its subsequent disturbance of the system) may be treated as independent events. Encroachments of a transition into the trailing edge of the response to a previous transition as a result of stimulus frequencies of 4 Hz or greater resulted in marked reduction of the response, as illustrated by the VEP waveforms shown in Fig. 4B. This suggests that in the cat VEP the adaptive impact of any transition is transient, with a duration on the order of 250 msec. The marked .attenuation of the VEP amplitude with temporal frequency also addresses the
issue of the origin of the VEP. Slow potentials such as the VEP are thought to arise primarily from post-synaptic-potential activity in the dendritic arborizations (e.g. Nunez, 1981). The extent to which the VEP reflects cortical activity, as opposed to signals from the lateral geniculate nucleus fibers of projection, remains unknown. In the cat, most retinal ganglion cells and geniculate cells have a broad temporal bandpass, often responding to Bicker in excess of 304OHz (e.g. Enroth-Cugell & Shapley, 1973). Cells in the cat visual cortex are by comparison sluggish, with the temporal cutoff frequency usually being limited to about 3-10 Hz (Movshon, Thompson & Tolhurst, 1978). The similarly sluggish bandpass seen in the VEP suggests that under our recording conditions it was primarily generated at cortical and/or more central levels. Because of the severe attenuation of the cat VEP at higher temporal frequencies, the use of frequencies beyond 2 Hz to study the cat VEP (e.g. Campbell et al., 1973) clearly deserves reconsideration. The effect of temporal modulation frequency on the relationship between VEP amplitude and log IAC 1 is shown in Fig. 4C. Higher temporal frequencies resulted in a reduced slope on this semilog scale, but the logarithmic nature of the stimulus-response relationship was not changed. Accompanying the reduction in the slope, an elevation of response threshold (intercept of the response line with the noise level) can also be seen. The reduction in response amplitude with temporal frequency is thus a result of a combination of reduced gain and elevated threshold. DISCUSSION
Static vs dynamic contrast The VEP responds solely to pattern transitions rather than static patterns. In our experiments, the cats were paralyzed and the eye movements suppressed. Once the presence of a base contrast was established, the static pattern would not itself generate a VEP response. Our interest was in whether the presence of a static base contrast modifies the VEP response to contrast increments, and our data suggest that is not the case. The VEP response system completely suppressed the standing contrast in favor of differential changes in contrast. If the eye movements were not controlled, however, a static contrast would become “dynamic” on the retina, and therefore could influence (or mask)
1514
X. D.
PANG
and A. B. BONDS
the VEP response to modulated contrast increments. This point is clarified by comparing our results with those from contrast modulation presented to alert subjects. Bodis-Wollner, Hendley and Kulikowski (1972) related VEP response to contrast modulation in the human, and found a dependence of the threshold for contrast modulation on base contrast. Since they were examining the threshold for detecting a change in contrast rather than the suprathreshold stimulusresponse relationship, we derived a threshold from our data for comparison. The justdetectable change-in-contrast, AC,, , is defined by the intercept of a linear extrapolation of the suprathreshold response with the noise level. Figure 3A shows that in the cat VEP, AC,, is essentially independent of base contrast. Since in behaving subjects the retinal image of a static contrast is really “dynamic”, it is not surprising that the mean contrast has an effect on contrastmodulation threshold. We feel, however, that their interpretation of the direction of the effect is open to question. They concluded that the contrast modulation threshold (which is not AC,,,; see below) decreases (or the “sensitivity” increases) monotonically as a function of the mean contrast, which was defined as the arithmetic mean of the contrasts before and after a grating transition. (Here we equate base contrast in our study with their mean contrast, since at threshold the difference is vanishingly small). In their study, a contrast modulation depth M was defined as M = AC/C_,, and the VEP contrast-modulation threshold Mth was defined as the intercept with zero voltage of the response amplitude as a function of M on a semilog scale. They plotted Mthvs C,,.,,,on a log-log scale and fitted a straight regression line, which had a negative slope, to the data. Such a relationship would mean a reduction in the modulation threshold (or an increase in “sensitivity”) as the mean contrast was increased. If their data are examined from the standpoint of AC,, rather than M,,,, however, a power law dependence of AC,, on C,,, with a positive exponent of about 0.85 emerges, meaning that AC,,, rises (or the sensitivity decreases) as C,,,,, rises. A subsequent study by the same group (Bobak et al., 1988) reaches a conclusion that is more compatible with the contrast masking data (for comparable background contrast) in the human (Kulikowski & Gorea, 1978; Legge & Foley, 1980) and behaving monkey (Smith et al.,
1982). Bobak et al. found that the suprathreshold slope of both the first and second harmonic frequency components of the VEP response became increasingly shallow with higher levels of mean contrast. Since the response level for the two components changed differently with mean contrast, they concluded that the effect was not due to fatigue or response suppression but rather to some form of contrast gain control. A positive dependence of threshold (or negative dependence of slope) on background level is analogous to masking of a tone by noise in the auditory system, since the refreshing of base contrast by eye movement is uncorrelated with contrast modulation. The higher the base or mean contrast, the stronger the “masking” effect. This explanation is also consistent with reports that the slope of the contrast masking function in behaving subjects is smaller for gratings with lower spatial frequencies (Kulikowski & Gorea, 1978; Smith et al., 1982) because gratings with lower spatial frequencies have lower slopes of luminance change and are thus likely to be less effectively refreshed by eye movement. Two issues that frequently rise in comparing results from anesthetized animals with that from awake humans are the use of anesthesia and difference in spatial resolution. It has been reported that when barbiturate doses several times higher than those involved in our study were used, contrast-mediated VEP response could be eliminated (but not altered) in the monkey (Padmos, Haaijman & Spekreijse, 1973; Van der Marel, Dagnelie & Spekreijse, 1981). Since we have always found a reliable and consistent VEP response to pattern transitions under our recording conditions [see Fig. 4(B)] and since our preparations yielded absolute contrast sensitivities comparable to those of the behaving cat (Berkley, 1990) we do not feel that our use of the anesthesia significantly compromised our results. It is known that the spatial frequency corresponding to the peak of contrast sensitivity for the cat is lower than that for the human by a factor of about 10 (Campbell et ,al., 1973). We selected spatial frequencies of 0.4 and 0.5 c/deg, which we found to be most effective for evoking maximum VEP responses in the range of 0.2-1.6 c/deg (Pang, 1983; Bonds, 1984), and which are lower than those used by Bodis-Wollner et al. (1972) and Bobak et al. (1988) in the human by a factor of about 10.
1515
VEP and contrast modulation in cat
Correlations with single-cell studies Ohzawa et al. (1982) reported a contrast adaptation mechanism in cat cortical cells. Elevation of the average contrast during an extended presentation (40 set) of a drifting grating reduced the cell’s response to gratings with different contrasts but otherwise identical to the background grating. This manifestation of gain control would imply a conflict with our failure to find one. However, stimulation conditions differed between the two experiments in two important aspects. First, for the single unit study, the adapting grating was constantly in motion, whereas for this VEP study the background contrast was static. Second, measurements reported here were not preceeded by a prolonged, effective, and constant stimulus, as in the single-unit study. After 30 set of contrast modulation at 1 Hz, we did, however, observe a reduction in the VEP response to contrast modulation of gratings which were identical to the adapting grating except for the level of the background contrast and change-in-contrast (Pang, 1983). The amount of reduction increased with the change-in-contrast of the adapting grating. The logarithmic stimulusresponse relationship was, like in the case of increasing temporal modulation frequency, retained. The adaptation was specific to the spatial frequency and orientation of the grating, with a recovery time of l-2 min. Similar results have been reported by Bonds (1984). This similarity in adaptability to prolonged stimuli between the VEP and cortical cell responses supports the notion that the VEP we recorded was generated at cortical or higher levels. Temporal effectiveness of contrast differentiation In the cat VEP the duration of the impact of any change in contrast was no longer than about 250 msec. After this period, even though contrast might remain, it had little impact on subsequent responses. While complete extinction of the effects of a background grating is not expected in psychophysical experiments due to eye motion, Wilson (1990) has reported a similar onset time course in contrast masking experiments. A 3 c/deg test pattern was superimposed on a similar mask at different onset asynchronies. Test pattern thresholds were elevated by a factor of 10 at 0 msec, but only by 4 after 200 msec. At onset the test threshold was a power function of masking contrast with an exponent of 0.69, whereas after 200msec the
exponent was reduced to 0.39. These observations are consistent with the idea that the impact of a mask dissipates over a period of no more than a few hundred milliseconds, with the exception that some masking component remains in the psychophysical domain, most probably as a result of motion of the retinal image. Functional signiJcance of the AC-VEP ship
relation-
In the experiments described here, the response as a function of change-in-contrast was independent of ambient contrast. Besides the factors discussed previously, an analysis of Fig. 1 may help to elaborate this point. The area of the shaded region in Fig. 1, i.e. the net change in light energy distribution over one spatial cycle resulting from a change in contrast, is: AA=2
‘(L;, s0
- L_)sin(x)
dx
= 4(AC)(L,,)
(9
which depends only on the change-in-contrast AC and the mean luminance [equation (4) is used in the calculation]. Thus, for a given AC, the amount of change in light energy distribution upon a contrast transition is independent on the base contrast C. The AC evoked response system may therefore be considered as a detector of changes in light energy distribution with essentially perfect a.c. coupling (i.e. responses are totally phasic). The consequences of a.c. coupling may be viewed in two ways: the response amplitude resulting from a change in contrast from, e.g. 30-40%, is identical to the amplitude resulting from an On-Off modulation of 10%. Acknowledging the logarithmic stimulus-response function, this is much larger than the difference between the response amplitudes resulting from a 30% and 40% On-Off modulation, respectively. A tendency to suppress static base contrasts thus enhances detection of small changes of suprathreshold contrast, but at the expense of the loss of information on absolute contrast levels. Alternatively, since the response to change-incontrast is independent of the base contrast, the a.c. coupling is not analogous to a Weber’s law mechanism. If threshold, or a just-detectable contrast modulation corresponds to a small, constant response amplitude, then it remains unchanged for all base contrasts. Thus in the contrast domain the Weber fraction (A&/C)
1516
X. D. PANGand A. B.
actually drops as the background contrast increases. A mechanism for the control of contrast gain is required because of the limited dynamic range of the visual cortex. One way of compensation is a nonlinear mapping of contrast to response, here evident in the logarithmic form of the relationship. Were this relationship to remain static, discrimination of different contrasts at or near threshold would be adequate, but discernible contrast increments would rise dramatically as background contrast rose. In cortical single units, a form of contrast gain control is evident from the rightward shift of the contrast-response function as contrast is increased, which keeps the log-linear portion of the response curve centered on the ambient contrast (Ohzawa et al., 1982). The a.c. differentiation found in the VEP performs essentially the same service, effectively resetting the operating point of the system back to zero (where increment sensitivity is high) despite the presence of a standing contrast. The effectiveness of this differentiation is illustrated by the absence of saturation in Fig. 3A. When a standing contrast also becomes “dynamic” on the retina as in behavioral studies, the resetting of the operating point will then not be perfect, as indicated by the reduced slope and saturation seen in suprathreshold VEP responses of human subjects exposed to increasing background contrasts (Bobak et al., 1988). Acknowledgemenf+-We thank Dr E. J. DeBruyn for his aid in animal preparations and Dr R. M. Held of MIT for commenting on an earlier version of the manuscript. A portion of this work was submitted by X. D. Pang as a master’s thesis to the Department of Electrical and Biomedical Engineering, Vanderbilt University, July 1983. This work was supported by the NIH grant EY03778-02 and the Vanderbilt University Research Council. Flaxedil was kindly provided by American Cyanamid.
REFERENCES
BONDS
Bobak, P., Bodis-Wollner, I. & Marx, M. (1988). Cortical contrast gain control in human spatial vision. Journal of Physiology,
London, 405, 421-437.
Bodis-Wollner, I., Hendley, C. D. & Kulikowski, J. J. (1972). Electrophysiological and psychophysical responses to modulation of contrast of a grating pattern. Perception,
I, 341-349.
Bonds, A. B. (1984). Spatial adaptation of the cortical visual evoked potential of the cat. Investigative Ophthalmology and Visual Science, 25, 640-646.
Campbell, evoked pattern. Campbell, contrast
F. W. & Kulikowski, J. J. (1972). The visual potential as a function of contrast of a grating Journal of Physiology,
ology, London, 233, 271-309.
Hammond, P. (1978). On the use of nitrous oxide/oxygen mixtures for anaesthesia in cats. Journal of Physiology, London, 275, 64.
Kulikowski, J. J. & Gorea, A. (1978). Complete adaptation to patterned stimuli: A necessary and sufficient condition to Weber’s law for contrast. Vision Research, 18, 1223-1227. Legge, G. E. & Foley, J. M. (1980). Contrast masking in human vision. JOWMI of the Optical Society of America, 70(12), 1458-1471.
Movshon, J. A., Thompson, I. D. & Tolhurst, D. J. (1978). Spatial and temporal sensitivity of neurons in area 17 and 18 of the cat’s visual cortex. Journal of Physiology, London, 283, 101-120.
Nunez, P. L. (1981). Electric fields of the brain. New York: Oxford University Press. Ohzawa, I., Sclar, G. & Freeman, R. D. (1982). Contrast gain control in the cat visual cortex. Nature, London, 298, 266268.
Padmos, P., Haaijman, J. J. & Spekreijse, H. (1973). Visually evoked cortical potentials to patterned stimuli in monkey and man. Electroencephalography and Clinical Neurophysiology 35, 153-166. Pang, X. D. (1983). Differential contrast gain control in the cat visual cortex. M.S. thesis, Department of Electrical and Biomedical Engineering, Vanderbilt University, Nashville, Tenn. Smith, E. L., Harweth, R. S., Levi, D. M. & Boltz, R. L. (1982). Contrast increment thresholds of rhesus monkeys. Vision Research, 22, 1153-I 161. Snyder, A. & Shapley, R. M. (1979). Deficits in the visual evoked potentials of cats as a result of visual deprivation. Experimental
Bain, R. & Kulikowski, J. J. (1976). Contrast thresholds for pattern and movement detection evaluated by evoked potentials. Journal of Physiology, London. 259, 3435. Berkley, M. A. (1990). Behavioral determination of the spatial selectivity of contrast adaptation in cats: Some evidence for a common plan in the mammalian visual system. Visual Neuroscience, 4, 413-426.
London, 222, 345-356.
F. W., Maffei, I. & Piccolino, M. (1973). The sensitivity of the cat. Journal of Physiology, London, 229, 7 19-73 1. Enroth-Cugell, C. & Shapley, R. M. (1973). Adaptation and dynamics of cat retinal ganglion cells. Journal of Physi-
Brain Research,
37, 73-86.
Van der Marel, H., Dagnelie, G. & Spekreijse, H. (1981). Pattern evoked potentials in awake rhesus monkeys. Investigative 457-466.
Ophthalmology
and
Visual
Science.
21.
Wilson, H. R. (1990). Psychophysics of contrast gain control. Investigative Ophthalmology and Visual Science (Suppl.),
31, 430.
