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Stephen Kuffler at a laboratory picnic, taken around 1965.



tween the receptors and bipolars, and amacrine cells between bipolars and retinal ganglion cells. (See the drawing of these direct and indirect connections on this page). These connections were already worked out in much detail by Ramon y Cajal around 1900. The direct path is highly specific or compact, in the sense that one receptor or only relatively few feed into a bipolar cell, and only one or relatively few bipolars feed into a ganglion cell. The indirect path is more diffuse, or extended, through wider lateral connections. The total area occupied by the receptors in the back layer that feed one ganglion cell in the front layer, directly and indirectly, is only about one millimeter. That area, as you may remember from Chapter i, is the receptive field of the ganglion cell, the region of retina over which we can influence the ganglion cell's firing by light stimulation.
This general plan holds for the entire retina, but the details of connections vary markedly between the fovea, which corresponds to exactly where we are looking—our center of gaze, where our ability to make out fine detail is highest—and the far outer reaches, or periphery, where vision becomes relatively crude. Between fovea and periphery, the direct part of the path from receptor to ganglion cell changes dramatically. In and near the fovea, the rule for the direct path is that a single cone feeds a single bipolar cell, and a single bipolar in turn feeds into one ganglion cell. As we go progressively farther out, however, more receptors converge on bipolars and more bipolars converge on ganglion cells. This high degree of convergence, which we find over much of the retina, together with the very compact pathway in and near the very center, helps to explain how there can be a 125:1 ratio of receptors to optic nerve fibers without our having hopelessly crude vision.
The general scheme of the retinal path, with its direct and indirect components, was known for many years and its correlation with visual acuity long recognized before anyone understood the significance of the indirect path. An understanding suddenly became possible when the physiology of ganglion cells began to be studied.


                        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 intermediate 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 behavior, 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 Hospital. 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 offcenter 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 spontaneous 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. Exploration 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 antagonistic 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 mistake 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.

   
 
 
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The two main types of retinal-ganglion-cell receptive fields are on center, with inhibitory surround, and off center, with excitatory surround. "+" stands for regions giving on responses, "—" for regions giving off responses.


 
 
 
 
 
A cross section of the retina, about midway between the fovea and far periphery, where rods are more numerous than cones.
From top to bottom is about one-quarter millimeter.


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Left: Four recordings from a typical oncenter retinal ganglion cell. Each record is a single sweep of the oscilloscope, whose duration is 2.5 seconds. For a sweep this slow, the rising and falling phases of the impulse coalesce so that each spike appears as a vertical line. To the left the stimuli are shown. In the resting state at the top, there is no stimulus: firing is slow and more or less random. The lower three records show responses to a small (optimum size) spot, a large spot covering the receptive-field center and surround, and a ring covering the surround only. Right: Responses of an offcenter retinal ganglion cell to the same set of stimuli shown at the left.