VISUAL ADAPTATION AND RETINAL GAIN CONTROLS
gain control on the product o f illumination and
area, we must revise equations (20) and (21) which
expressed the gain in terms of illumination. The
earlier equations were correct under the conditions
of full field illumination when the entire receptive
field would be covered by the uniform background.
In this case the gain would just be scaled down by
a factor equal to the area of the center of the
receptive field. But a more general equation can be
written which applies to backgrounds of any spatial
configuration. For the rod pathway:
GR = GR0/(1 + FB/FRo)p (24)
and a similar equation describes the gain of the cone
pathway, G o Flux is illumination multiplied by
area, in this case the total summing area of the
center of the receptive field. For step responses, the
exponent P has the value 0.9 for the rod pathway
and is somewhat higher for the cone pathway. What
equation (24) means is that the gain depends on
background flux, F B, not retinal illumination, flux
added up over the entire center of the receptive field
and weighted by the distribution of sensitivity of
the receptive field center. Also, the adapting flux
has to exceed a critical value, denoted FRO for the
scotopic system, in order for the cell to undergo the
transition from dark adaptation to light adaptation.
It may help to conceive of this critical flux as the
background flux required to produce a critical level
of D.C. neural signal which, when exceeded, turns
on the retinal gain control. The value of the critical
flux, FRO, is about 104 quanta s -1 at the retina on
the average (Enroth-Cugell and Shapley, 1973b).
3.5.2. LOCAL AND GLOBAL GAIN CONTROLS WHICH
DEPEND ON FLUX
Further investigation of the spatial summation of
adaption in cat ganglion cells was performed by
Harding (1977). One of his major results is
illustrated in Fig. 35. The experiment was designed
to measure the spatial weighting of adaptation with
a two-spot paradigm: one test and one adapting
spot. The test spot was fixed in position in the
middle of the receptive field. Then the position of
the adapting spot was varied and its luminance
adjusted so that the gain of the response to the test
was reduced by a criterion amount. In the same cells
the sensitivity profile for eliciting a response was
309
also measured. This latter profile is called the signal
sensitivity profile. As can be seen from the results
in Fig. 35, the signal sensitivity profile and the
adaptation profile were approximately the same in
X cells. In some Y cells the gain reduction for a test
spot near the adapting spot was greater than for a
test spot farther from the adapting spot, by more
than would be predicted from the Y cell's signal
sensitivity profile. That is, there were indications
of local adaptation in the Y cell center. A similar
sort of effect was seen in an investigation of light
adaptation of the receptive field surround of Y cells
(Cleland et al., 1973). There is thus evidence for two
different gain controls in the Y cell center: one local,
one more global. There is also evidence for local
adaptation in some X cells (Harding, 1978). A
discussion of the implications of these experiments
for X / Y receptive field organization would carry
us too far from the central issues of this paper. But
a brief comment about these different adaptation
profiles in X and Y cells may provoke some thought
a b o u t the retinal microcircuitry underlying
adaptation.
It is known that at any retinal locus the receptive
field centers of X cells are about ten times smaller
in area than those of Y cells (Hochstein and
Shapley, 1976b; Cleland et al., 1979; So and
Shapley, 1979; Linsenmeier et al., 1982). There exist
subunits of the Y cell's receptive field which are
roughly the same size as X cell centers at the same
retinal eccentricity (Hochstein and Shapley, 1976b;
So and Shapley, 1979; cf. Appendix 2). It has been
suggested that X cell centers and Y cell subunits are
approximately determined by the spatial summing
areas of bipolar cells (Hochstein and Shapley,
1976b; Victor and Shapley, 1979). While recent
neuroanatomical investigation of the retina suggests
this is only an approximation to the actual situation,
it seems now to be an approximation rather than
mere speculation (see Sterling, 1983). Thus, if one
accepts our previous assertion that the interneuron
which determines the size of the X cell's center must
set the gain of the center, then the bipolar cells must
control the gain of the X center, in some way. If
these same bipolar cells feed into the Y cells'
subunits, one must suppose they control the gain
of the subunits. The local effects o f gain reduction
in Y cells seen in Fig. 35 could be explained by this
" b i p o l a r " gain control, which we infer to be