THE RECEPTIVE FIELDS OF
                           RETINAL GANGLION CELLS:
                              THE OUTPUT OF THE EYE
In studying the retina we are confronted with two main problems:
First, how do the rods and cones translate the light they receive into electrical,
and then chemical, signals? Second, how do the subsequent cells in the next
two layers—the bipolar, horizontal, amacrine, and ganglion cells—interpret
this information? Before discussing the physiology of the receptors and inter-
mediate cells, I want to jump ahead to describe the output of the retina—
represented by the activity of the ganglion cells. The map of the receptive field
of a cell is a powerful and convenient shorthand description of the cell's behav-
ior, and thus of its output. Understanding it can help us to understand why the
cells in the intermediate stages are wired up as they are, and will help explain
the purpose of the direct and indirect paths. If we know what ganglion cells are
telling the brain, we will have gone far toward understanding the entire retina.
Around 1950, Stephen Kuffler became the first to record the responses of
retinal ganglion cells to spots of light in a mammal, the cat. He was then
working at the Wilmer Institute of Ophthalmology at the Johns Hopkins Hos-
pital. In retrospect, his choice of animals was lucky because the cat's retina
seems to have neither the complexity of movement responses we find in the
frog or rabbit retina nor the color complications we find in the retinas of fish,
birds, or monkeys. Kuffler used an optical stimulator designed by Samuel
Talbot. This optical device, a modified eye doctor's ophthalmoscope, made it
possible to flood the retina with steady, weak, uniform background light and
also to project small, more intense stimulus spots, while directly observing
both the stimulus and the electrode tip. The background light made it possible
to stimulate either rods or cones or both, because only the cones work when
the prevailing illumination is very bright, and only the rods work in very dim
light. Kuffler recorded extracellularly from electrodes inserted through the
sclera (white of the eye) directly into the retina from the front. He had little
difficulty finding retinal ganglion cells, which are just under the surface and are
fairly large.
With a steady, diffuse background light, or even in utter darkness, most
retinal ganglion cells kept up a steady, somewhat irregular firing of impulses,
at rates of from 1to 2 up to about 20 impulses per second. Because one might
have expected the cells to be silent in complete darkness, this firing itself came
as a surprise.
By searching with a small spot of light, Kuffler was able to find a region in
the retina through which he could influence—increase or suppress—the retinal
ganglion cell's firing. This region was the ganglion cell's receptive field. As
you might expect, the receptive field was generally centered at or very near the
tip of the electrode. It soon became clear that ganglion cells were of two types,
and for reasons that I will soon explain, he called them on-center cells and off-
center cells. An on-center cell discharged at a markedly increased rate when a
small spot was turned on anywhere within a well-defined area in or near the
center of the receptive field. If you listen to the discharges of such a cell over a
loudspeaker, you will first hear spontaneous firing, perhaps an occasional
click, and then, when the light goes on, you will hear a barrage of impulses
that sounds like a machine gun firing. We call this form of response an on
response. When Kuffler moved the spot of light a small distance away from the
center of the receptive field, he discovered that the light suppressed the sponta-
neous firing of the cell, and that when he turned off the light the cell gave a
brisk burst of impulses, lasting about i second. We call this entire sequence—
suppression during light and discharge following light—an off response. Explo-
ration of the receptive field soon showed that it was cleanly subdivided into a
circular on region surrounded by a much larger ring-shaped off region.

 

 

 

 

 

 

The more of a given region, on or off, the stimulus filled, the greater was
the response, so that maximal on responses were obtained to just the right size
circular spot, and maximal off responses to a ring of just the right dimensions
(inner and outer diameters). Typical recordings of responses to such stimuli are
shown on this page. The center and surround regions interacted in an antago-
nistic way: the effect of a spot in the center was diminished by shining a second
spot in the surround—as if you were telling the cell to fire faster and slower at
the same time. The most impressive demonstration of this interaction between
center and surround occurred when a large spot covered the entire receptive
field of the ganglion cell. This evoked a response that was much weaker than
the response to a spot just filling the center; indeed, for some cells the effects of
stimulating the two regions cancelled each other completely.
An off-center cell had just the opposite behavior. Its receptive field consisted
of a small center from which off responses were obtained, and a surround that
gave on responses. The two kinds of cells were intermixed and seemed to be
equally common. An off-center cell discharges at its highest rate in response to
a black spot on a white background, because we are now illuminating only the
surround of its receptive field. In nature, dark objects are probably just as
common as light ones, which may help explain why information from the
retina is in the form of both on-center cells and off-center cells.
If you make a spot progressively larger, the response improves until the
receptive-field center is filled, then it starts to decline as more and more of the
surround is included, as you can see from the graph on the next page. With a
spot covering the entire field, the center either just barely wins out over the
surround, or the result is a draw. This effect explains why neurophysiologists
before Kuffler had such lack of success: they had recorded from these cells but
had generally used diffuse light—clearly far from the ideal stimulus.
   You can imagine what a surprise it must have been to observe that shining a
flashlight directly into the eye of an animal evoked such feeble responses or no
response at all. Illuminating all the receptors, as a flashlight surely does, might
have been expected to be the most effective stimulus, not the least. The mis-
take is to forget how important inhibitory synapses are in the nervous system.
With nothing more than a wiring diagram such as the one on page 7, we
cannot begin to predict the effects of a given stimulus on any given cell if we
do not know which synapses are excitatory and which are inhibitory. In the
early 1950s, when Kuffler was recording from ganglion cells, the importance
of inhibition in the nervous system was just beginning to be realized.