VISUAL ADAPTATION AND RETINAL GAIN CONTROLS
from Enroth-Cugell and Lennie (1975) reveals the
kinds of surround adaptation which are seen. In
these experiments, the surround response was
estimated by subtracting the center response from
that obtained by illumination of both center and
surround. The data are the incremental illumination
required to elicit a criterion surround response; thus
these curves may be interpreted as indications of
changes in surround gain with background
illumination. In the upper panel, the surround and
center begin to reduce their gains together at
roughly the same level of background. In the lower
panel the surround starts off with a lower dark-
adapted gain, but reduces its gain with background
at a higher level than the center. The result is that
in both cases the center and surround have roughly
the same gains (integrated over their respective total
summing areas) in the Weber-Law, light adapted
scotopic range. But there are differences across the
population of retinal ganglion cells in the relative
gain of center and surround in the low scotopic
range (see also Kaplan et al., 1979).
The results of the well-known investigation of
Barlow et al. (1957) are sometimes interpreted to
mean that the gain of the surround goes to zero in
total dark adaptation. This, however, is not
precisely what Barlow et al. found. Their results on
the dependence of gain on area at different
backgrounds implied that the ratio of the gain of
the center to the gain of the surround increased in
total dark adaptation. However, the extent of the
increase in the c e n t e r - s u r r o u n d ratio was not
determined in their study. It was later shown by
Enroth-Cugell and Lennie (1975) and by Kaplan et
al. (1979) that this ratio may increase from a value
of 1.2 in the light adapted state to as much as 3 in
the dark adapted state. That is, the surround is
relatively weaker compared to the center in the
dark, but it is not gone. In fact, the gain of the
surround is always maximal when the retina is dark
adapted (see Fig. 26). In other words, as the
background level is increased from total darkness,
the center gain usually is reduced at a lower level
of background than is the surround's gain.
There is a methodological reason for the
differences in conclusions about the strength of the
surround in the dark. Barlow et al. (1957) used
auditory threshold for an "off-response" to
measure the magnitude of the response of the
301
surround in on-center cells. This method has the
disadvantage that, in these cells, the surround
response consists of sustained inhibition when the
surround mechanism is dark adapted (Enroth-
Cugell and Lennie, 1975). The presence and
magnitude of the "off-response" is associated with
the adaptation level, just as the magnitude of the
center's transient overshoot depends on the center
being somewhat light-adapted (see Fig. 25). Enroth-
Cugell and Lennie (1975) and Kaplan et al. (1979)
measured magnitude of inhibition as an indicator
of surround response strength, and they did it with
objective averaging techniques. Their work reveals
that there are marked variations across the
population of ganglion cells in the degree to which
background illumination affects the ratio of the
center and surround gains (see Fig. 26). The finding
of variability in the degree of center-surround
balance in the dark has also been reported by
Barlow and Levick (1976).
The fact that background light in the scotopic
range can affect the gains of center and surround
differently implies that, in this range, the gains of
these receptive field mechanisms are controlled at
a site (or sites) in the retina more proximal than the
photoreceptors. If the only site of gain reduction
were the photoreceptors, one would observe that
the gains of center and surround would begin to
drop at the same background level. There is good
evidence that at higher backgrounds some of the
reduction in gain in the mammalian retina is due
to photoreceptor adaptation (Sakmann and Filion,
1972; Valeton and van Norren, 1983). These
observations are consistent with our assertion in the
Introduction that there is a hierarchy of gain
controls.
The ratio of the total integrated gains of center
and surround in the light-adapted state is
approximately 1.2 for a large population of retinal
ganglion cells (Linsenmeier et al., 1982). There is
considerable variance in this ratio among the
ganglion cell population. In any one cell, the ratio
is approximately constant from 10-2-5cd m -2 back-
ground luminance on up (Enroth-Cugell and
Lennie, 1975). Thus, in cat ganglion cells the
balance between center and surround is established
in the low- to mid- scotopic range and is invariant
with adaptation level throughout the mid- to high°
scotopic and photopic ranges.