VISUAL ADAPTATION AND RETINAL GAIN CONTROLS
Furthermore, the phase curves at different contrasts
would be superimposable. This is not the case. The
amplitude curve is shifted towards higher temporal
frequencies at higher contrasts, and the phases of
intermediate frequencies are advanced at higher
contrasts. At an r.m.s, average contrast of 0.2, the
amplitude of the response to 0.5 Hz may be reduced
by 50°7o on account of the action of the contrast
gaincontrol. The phase may be shifted at 8 Hz by
as much as 60 deg. Another way to look at the
contrast gaincontrol is that it produces what appears
to be a f r e q u e n c y - d e p e n d e n t saturation. The
amplitudes of responses to higher temporal
frequencies grow approximately proportionally with
contrast. The amplitudes of responses to lower
temporal frequencies grow less than proportionally
with contrast, and appear to saturate at a lower
contrast. That this effect is not simple saturation
is proven by the temporal frequency dependence.
The spatial and temporal dependence of the
contrast gaincontrol's action indicate that it has the
same characteristics as the nonlinear receptive field
subunits which feed excitation to Y cells (Shapley
and Victor, 1978; cf. Appendix 2). It appears that
the subunits precede the contrast gaincontrol in
retinal processing; the subunits compute the total
average contrast which is then used to control
the retina's dynamic responses. The way that the
contrast gaincontrol modifies the time course of
retinal responses appears to be by modulation of
the strength of pre-existing feedback pathways.
That is, increase of contrast tends to turn on the
contrast gaincontrol which then increases the
strength of negative feedback in both X and Y
retinal pathways (Shapley and Victor, 1981).
The contrast gaincontrol calculates a contrast
signal by averaging the contrast modulation over
a wide expanse of retina. The spatial extent of the
area of contrast averaging has not been determined
precisely, but it must be considerably larger than
the extent of the center mechanism of Y ganglion
cells. Rough estimates of its spatial extent may be
based on the area over which the product, contrast
times area, produces a given amount of low
frequency suppression or mid-frequency phase
advance. This area is on the order of ten degrees,
i.e. about 2 mm on the retina. Furthermore, the
contrast gaincontrol may receive weaker but still
significant input from still further reaches of the
317
retina, in this way also resembling the excitatory
nonlinear subunits of Y cells. Thus the contrast
gaincontrol must involve a third type of interneuron
different from the previously inferred interneurons
which are needed to account for the flux
gaincontrols of the X and Y cell center mechanisms.
Because of its wide summing area, the contrast
gaincontrol can account for nonlinear spatial
summation of responses produced by contrast
modulation in the center and periphery of X and
Y ganglion cell receptive fields (Shapley and Victor,
1979). This has been observed with sinusoidal test
stimuli by Shapley and Victor and with square wave
Y CELL
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TEMPORAL FREQUENCY
FIG. 41. The contrast gaincontrol revealed in temporal
frequency responses o f retinal ganglion cells. These are data
from an on-center Y cell. The mean luminance was 20 cd m -2,
and the pupil diameter was 3 m m . The stimulus was a 0.25
c deg-' sine grating which was modulated in amplitude by
a s u m of sinusoids, with temporal frequencies from 0.2 up
to 32 Hz. The empty circles were obtained when the contrast
was 0.0125 per sinusoid, i.e. if any one of the eight sinusoids
had been presented alone, the peak contrast of the modulated
grating would have been 0.0125. The filled circles were
obtained with 0.1/sinusoid contrast. The amplitudes plotted
are the Fourier amplitudes in the cell's impulse train which
were at the temporal frequencies present in the stimulus; the
phases are the phase shifts o f those Fourier components in
the impulse train with respect to the corresponding
c o m p o n e n t in the input signal. If the retina were linear, or
if the nonlinearity were a simple saturation, the two amplitude
curves should be parallel, and the phase curves should be
parallel, and the phase curves should superimpose. The
accentuation of responses at high frequencies, and the phase
advance at mid-range frequencies, as contrast increases, is
the signature o f the contrast gaincontrol. From Shapley and
Victor (1979).