the sweeping had to be done with the edge in one particular orientation. Most amazing was the contrast between the machine-gun discharge when the orientation of the stimulus was just right and the utter lack of a response if we changed the orientation or simply shined a bright flashlight into the cat's eyes.
The discovery was just the beginning, and for some time we were very confused because, as luck would have it, the cell was of a type that we came later to call complex, and it lay two stages beyond the initial, center-surround cortical stage. Although complex cells are the commonest type in the striate cortex, they are hard to comprehend if you haven't seen the intervening type.
Beyond the first, center-surround stage, cells in the monkey cortex indeed respond in a radically different way. Small spots generally produce weak responses or none. To evoke a response, we first have to find the appropriate part of the visual field to stimulate, that is, the appropriate part of the screen that the animal is facing: we have to find the receptive field of the cell. It then turns out that the most effective way to influence a cell is to sweep some kind of line across the receptive field, in a direction perpendicular to the line's orientation. The line can be light on a dark background (a slit) or a dark bar on a white background or an edge boundary between dark and light. Some cells prefer one of these stimuli over the other two, often very strongly; others respond about equally well to all three types of stimuli. What is critical is the orientation of the line: a typical cell responds best to some optimum stimulus orientation; the response, measured in the number of impulses as the receptive field is crossed, falls off over about 10 to 20 degrees to either side of the optimum, and outside that range it declines steeply to zero (see the illustration on the facing page). A range of 10 to 20 degrees may seem imprecise, until you remember that the difference between one o'clock and two o'clock is 30 degrees. A typical orientation-selective cell does not respond at all when the line is oriented 90 degrees to the optimal.
Unlike cells at earlier stages in the visual path, these orientation-specific cells respond far better to a moving than to a stationary line. That is why, in the diagram on the facing page, we stimulate by sweeping the line over the receptive field. Flashing a stationary line on and off often evokes weak responses, and when it does, we find that the preferred orientation is always the same as when the line is moved.
In many cells, perhaps one-fifth of the population, moving the stimulus brings out another kind of specific response. Instead of firing equally well to both movements, back and forth, many cells will consistently respond better to one of the two directions. One movement may even produce a strong response and the reverse movement none or almost none, as illustrated m the figure on the facing page.
In a single experiment we can test the responses of 200 to 300 cells simply by learning all about one cell and then pushing the electrode ahead to the next cell to study it. Because once you have inserted the delicate electrode you obviously can't move it sideways without destroying it or the even more delicate cortex, this technique limits your examination to cells lying in a straight line.
Fifty cells per millimeter of penetration is about the maximum we can get with present methods. When the orientation preferences of a few hundred or a thousand cells are examined, all orientations turn out to be about equally represented—vertical, horizontal, and every possible oblique. Considering the nature of the world we look at, containing as it does trees and horizons, the question arises whether any particular orientations, such as vertical and horizontal, are better represented than the others. Answers differ with different laboratory results, but everyone agrees that if biases do exist, they must be small—small enough to require statistics to discern them, which may mean they are negligible!
In the monkey striate cortex, about 70 to 80 percent of cells have this property of orientation specificity. In the cat, all cortical cells seem to be orientation selective, even those with direct geniculate input.
We find striking differences among orientation-specific cells, not just in optimum stimulus orientation or in the position of the receptive field on the retina, but in the way cells behave. The most useful distinction is between two classes of cells: simple and complex. As their names suggest, the two types differ in the complexity of their behavior, and we make the reasonable assumption that the cells with the simpler behavior are closer in the circuit to the input of the cortex.
For the most part, we can predict the responses of simple cells to complicated shapes from their responses to small-spot stimuli. Like retinal ganglion cells, geniculate cells, and circularly symmetric cortical cells, each simple cell has a small, clearly delineated receptive field within which a small spot of light produces either on or off responses, depending on where in the field the spot falls. The difference between these cells and cells at earlier levels is in the geometry of the maps of excitation and inhibition. Cells at earlier stages have maps with circular symmetry, consisting of one region, on or off, surrounded by the opponent region, off or on. Cortical simple cells are more complicated. The excitatory and inhibitory domains are always separated by a straight line or by two parallel lines, as shown in the three drawings on this page. Of the various possibilities, the most common is the one in which a long, narrow region giving excitation is flanked on both sides by larger regions giving inhibition, as shown in the first drawing (a).
To test the predictive value of the maps made with small spots, we can now try other shapes. We soon learn that the more of a region a stimulus fills, the stronger is the resultant excitation or inhibition; that is, we find spatial summation of effects. We also find antagonism, in which we get a mutual cancellation of responses on stimulating two opposing regions at the same time. Thus for a cell with a receptive-field map like that shown in the first drawing (a), a long, narrow slit is the most potent stimulus, provided it is positioned and oriented so as to cover the excitatory part of the field without invading the inhibitory part (see the illustration on the facing page). Even the slightest misorientation causes the slit to miss some of the excitatory area and to invade the antagonistic inhibitory part, with a consequent decline in response.
In the second and third figures (b and c) of the diagram on this page, we see two other kinds of simple cells: these respond best to dark lines and to dark/
light edges, with the same sensitivity to the orientation of the stimulus. For all three types, diffuse light evokes no response at all. The mutual cancellation is obviously very precise, reminiscent of the acid-base titrations we all did in high school chemistry labs. Already, then, we can see a marked diversity in cortical cells. Among simple cells, we find three or four different geometries, for each of which we find every possible orientation and all possible visualfield positions.
The size of a simple-cell receptive field depends on its position in the retina relative to the fovea, but even in a given part of the retina, we find some variation in size. The smallest fields, in and near the fovea, are about onequarter degree by one-quarter degree in total size; for a cell of the type shown in diagrams a or b in the figure on this page, the center region has a width of as little as a few minutes of arc. This is the same as the diameters of the smallest receptive-field centers in retinal ganglion cells or geniculate cells. In the far retinal periphery, simple-cell receptive fields can be about 1 degree by 1 degree.
Even after twenty years we still do not know how the inputs to cortical cells are wired in order to bring about this behavior. Several plausible circuits have been proposed, and it may well be that one of them, or several in combination, will turn out to be correct. Simple cells must be built up from the antecedent cells with circular fields; by far the simplest proposal is that a simple cell receives direct excitatory input from many cells at the previous stage, cells whose receptive-field centers are distributed along a line in the visual field, as shown in the diagram on the next page.
It seems slightly more difficult to wire up a cell that is selectively responsive to edges, as shown in the third drawing (c) on the facing page. One workable scheme would be to have the cell receive inputs from two sets of antecedent cells having their field centers arranged on opposite sides of a line, on-center cells on one side, off-center cells on the other, all making excitatory connections. In all these proposed circuits, excitatory input from an off-center cell is logically equivalent to inhibitory input from an on-center cell, provided we assume that the off-center cell is spontaneously active.
Working out the exact mechanism for building up simple cells will not be easy. For any one cell we need to know what kinds of cells feed in information—for example, the details of their receptive fields, including position, orientation if any, and whether on or off center—and whether they supply excita
Various stimulus geometries evoke different responses in a cell with receptive field of the type in diagram a of the previous figure. The stimulus line at the bottom indicates when the slit is turned on and, i second later, turned off. The top record shows the response to a slit of optimum size, position, and orientation. In the second record, the same slit covers only part of an inhibitory area. (Because this cell has no spontaneous activity to suppress, only an off discharge is seen.) In the third record, the slit is oriented so as to cover only a small part of the excitatory region and a proportionally small part of the inhibitory region; the cell fails to respond. In the bottom record, the whole receptive field is illuminated; again, there is no response.
Responses of one of the first orientationspecific cells Torsten Wiesel and I recorded, from a cat striatc cortex in 1958. This cell not only responds exclusively to a moving slit in an eleven o'clock orientation but also responds to movement right and up, but hardly at all to movement left and down.
Three typical receptive-field maps for simple cells. The effective stimuli for these cells are (a) a slit covering the plus (+) region, (b) a dark line covering the minus (—) region, and (c) a light-dark edge falling on the boundary between plus and minus.