322 R. M . SHAPLEY AND C.
ENROTH-CUGELL
the right as would follow from gain re-adjustment
by illumination of the surround (see Section 1.2.2.).
Control experiments established that this was not
a result of light scatter onto the center (Werblin
1974). This is evidence that, in the mudpuppy
retina, the gain of the bipolar cell is set by signals
coming from its surround, which in this species is
believed to be mediated by horizontal cells (Werblin
and Dowling, 1969; Thibos and Werblin, 1978a).
Such results suggest that, in the mudpuppy,
horizontal cells act as a gain control on bipolar cells.
Two points of comparison with previously
presented psychophysical and physiological results
are needed here, to prevent the (probably erroneous)
inference that this conclusion is generally applicable
to all vertebrates.
The first comparison of Fig. 47 is with the
sensitization p h e n o m e n o n in human vision
discovered by Westheimer (1965). The results in
Fig. 47 are the opposite o f W e s t h e i m e r
sensitization. Illumination in the periphery of the
mudpuppy bipolar's receptive field desensitizes the
center in Werblin's (1974) and Thibos' and
Werblin's (1978a) experiments. There is, however,
a puzzling and unresolved contradiction with
Burkhardt's (1974) report of sensitization in
mudpuppy bipolar cells. Perhaps it has to do with
different receptor input to the bipolar cells in the
two sets of experiments. Thibos and Werblin
(1978a) were working at low backgrounds at which
rods were the predominant input while Burkhardt
was working with a highly light adapted mudpuppy
retina in which it is probable that cones were the
predominant photoreceptor inputs to the proximal
retinal neurons. If this is the explanation for the
opposite results, it would be an interesting and
unusual example of a reversal in functional
characteristics because of the transition from rod
to cone pathways.
A second comparison worth pursuing is that
between the strong effect on the gain of the center
exerted by the surround of mudpuppy bipolar cells
(Fig. 47) vis-a-vis negligible or, at most, weak effect
of the surround on the gain of the center in X and
Y cat retinal ganglion cells (Figs 3 8 - 4 0 ) . This
difference between results on the spatial extent of
"adaptation pools" suggests that quite different
mechanisms are involved in the control of gain in
the mudpuppy and cat retinas. In a sense such a
difference would not be surprising because the
mudpuppy and cat have evolved quite differently
with widely different visual capacities. The details
of exactly how the retinal network is connected
spatially to regulate gain might well differ between
two such distantly related animals.
Ashmore and Falk (1980) have demonstrated that
the gain of bipolar cells, in the almost all-rod retina
of the dogfish, begins to drop at extremely low
backgrounds because of saturation in the bipolar
cell itself. In the dogfish retina, there is a very high
amplification of rod signals at the rod-bipolar
synapse, and as a result the bipolar cells approach
their response ceilings at very low backgrounds.
There is no evidence for a gain control, and
t h e r e f o r e true light a d a p t a t i o n , in these
experiments. However, the results of Werblin (1974)
and Naka et al. (1979) illustrate how an automatic
gain control, acting on signals from photoreceptors
to bipolar cells, staves off saturation in mudpuppy
and catfish bipolars. In Fig. 46 for example, the
catfish bipolar's gain begins to drop at a lower mean
level than the horizontal cell's gain, presumably due
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FIG. 47. The effect of a steady illumination in the periphery
of the receptive field on the stimulus - response function of
mudpuppy bipolar cells; intracellular recording. The stimulus
was a flashing spot centered on the receptive field of the
bipolar cell. The spot's diameter, 0.4 m m , was chosen to
stimulate the center optimally. Stimulus duration was 1 s.
The response measure was the steady state plateau of the 1 s
response. Filled circles are for no illumination in the periphery
o f the receptive field; empty circles are response magnitudes
when a - 4 log unit steadily illuminated annulus was placed
in the periphery of the field. A modified N a k a - R u s h t o n
function was fitted to the data in the condition of no
peripheral illumination, and then translated laterally to fit
the results obtained with the annulus. The light source was
a tungsten lamp, attenuated by neutral filters. The
unattenuated retinal illumination was calculated to be about
10'3 quanta(522 nm) (cm ~ s)-t. Illuminations are given as log
attenuation relative to this value. From Thibos and Werblin
(1978a).