306 R . M . SHAPLEY AND C .
E N R O T H - C U G E L L
100
10
i expected. F u r t h e r m o r e , there is evidence for pooling
IIII 1 1 i IIIIII I I 1111111
001 0+1 1 o f a d a p t i v e signals over the entire center o f the
S p a t i a l f r e q u e n c y (c/deg)
FIG. 31. The effect of mean luminance on the dependence
of a ganglion cell's contrast gain on spatial frequency. Four
mean luminance levelswere used: 16 (empty circles), 0.5 (f'dled
triangles), 1.6" 10-2 (filled circles), and 5" 10-4 cd m-2 (empty
triangles). The highest mean luminance corresponds to
approximately 108 quanta(507 nm) (deg2 s)-1 retinal
illumination. What we have called "contrast gain" is labeled
"contrast sensitivity" in the figure. A 3.5 mm diameter
artificial pupil was used. The criterion response was audible
impulse rate modulation at the drift rate of the grating, 4 Hz.
The data were fit with smooth curves calculated from a
Difference of Gaussians model, where the smaller Gaussian
represents the receptive field center. The estimated diameter
of the center changed by about a factor of two over the range
of mean luminances studied. The cell studied here was an
on-center X cell. From Enroth-Cugell and Robson (1966).
a w a y to forge a s t r o n g e r link between the
m i c r o c i r c u i t r y o f the retina a n d its function. In a n y
case, the d a t a on the relatively small changes o f
receptive field center size with b a c k g r o u n d or m e a n
level serve to reinforce even m o r e s t r o n g l y the
c o n c l u s i o n t h a t signals f r o m d i f f e r e n t parts o f the
receptive field center a d a p t t o g e t h e r a n d with
a p p r o x i m a t e l y the same slope o n the gain vs
b a c k g r o u n d curve.
3.5. Adaptational Pooling and Receptive Field Size
3.5.1. SIGNAL POOLS AND ADAPTATIONPOOLS
I n v e s t i g a t i o n o f the s p a t i a l s u m m a t i o n o f
desensitization by a d a p t i n g lights is i m p o r t a n t for
an u n d e r s t a n d i n g o f the functions a n d m e c h a n i s m s
o f light a d a p t a t i o n . As we discussed in Sections
1.2.1. a n d 2.1.6. in c o n n e c t i o n with the ideas o f
Whittle and Challands, Land and McCann,
R u s h t o n , a n d W e s t h e i m e r , the s p a t i a l s u m m a t i o n
o f retinal a d a p t i v e signals has been inferred f r o m
psychophysical experiments. Furthermore,
questions a b o u t the influence o f b a c k g r o u n d light
at one place in the visual field on the response to
a test light at a n o t h e r place have been raised in
theories o f vision by ( a m o n g others) H e r i n g (1920),
H e l s o n (1964), Sperling (1970), a n d G r o s s b e r g
(1981). A wealth o f p h y s i o l o g i c a l results s u p p o r t s
the c o n c e p t o f a d a p t a t i o n a l p o o l i n g , b u t indicates
t h a t the p o o l s are smaller t h a n m o s t theorists have
receptive field, a n d also m o r e localized a d a p t i v e
p o o l i n g in sub-regions o f the receptive field center
a n d s u r r o u n d . H o w e v e r , in the cat, s t e a d y
i l l u m i n a t i o n o f the s u r r o u n d has little or no effect
on the gain o f the center.
In the cat retina, the gain o f the center mechanism
o f the receptive field o f a retinal g a n g l i o n cell is
d e t e r m i n e d by the sum o f all the steady light falling
on the center, a n d only on the center. This has been
proven by a n u m b e r o f different experiments which
are consistent with each other. T h e first was the
e x p e r i m e n t o f C l e l a n d a n d E n r o t h - C u g e l l (1968),
the results o f which are s h o w n in Fig. 32. In this
e x p e r i m e n t , the signal summation area was
m e a s u r e d with stimulus disks o f v a r i o u s areas.
I l l u m i n a t i o n was a d j u s t e d to give a c o n s t a n t
criterion response. Ricco's Law held a p p r o x i m a t e l y
for disk areas less t h a n the signal s u m m a t i o n area,
i . e . I . A - - k R s , where kRs is the c o n s t a n t for Ricco
signal s u m m a t i o n . F o r areas larger t h a n the signal
s u m m a t i o n area, R i c c o ' s L a w no longer held a n d
a c o n s t a n t i l l u m i n a t i o n was r e q u i r e d to elicit a
criterion response. The area over which Ricco's Law
held was e q u a t e d with the c e n t e r ' s a r e a o f signal
s u m m a t i o n . F o r the s a m e cell the adaptive
summation area was d e t e r m i n e d , a g a i n with a
c o n s t a n t response criterion. In this case, a r e a a n d
i l l u m i n a t i o n o f an a d a p t i n g disk were varied
r e c i p r o c a l l y in o r d e r t h a t the g a n g l i o n cell w o u l d
p r o d u c e a c o n s t a n t response to the test spot. The
test spot was c o n s t a n t in a r e a a n d i l l u m i n a t i o n ; it
was placed in the center o f the receptive field.
A d a p t i v e s u m m a t i o n followed Ricco's L a w also for
disks with areas less t h a n the a d a p t i v e s u m m a t i o n
area. That is, for a d a p t a t i o n , I . A = kRA, where kRA
is the c o n s t a n t for Ricco a d a p t i v e s u m m a t i o n . F o r
larger disks, s u m m a t i o n o f a d a p t i v e sensitivity