The overlap and blurring of ocular-dominance columns beyond layer 4 is due to horizontal or diagonal connections.
VARIATIONS IN COMPLEXITY
As we would expect, cells near the input end of the cortex, in layer 4, show less complicated behavior than cells near the output. In the monkey, as noted in this chapter, cells in layer 4C Bata, which receive input from the upper four (parvocellular) geniculate layers, all seem to have center-surround properties, without orientation selectivity. In layer 4C alpha, whose input is from the ventral (magnocellular) pair of geniculate layers, some cells have centersurround fields, but others seem to be orientation-specific, with simple receptive fields. Farther downstream, in the layers above and below 4C, the great majority of cells are complex. End-stopping occurs in about 20 percent of cells in layers 2 and 3 but seldom occurs elsewhere. On the whole, then, we find a loose correlation between complexity and distance along the visual path, measured in numbers of synapses.
Stating that most cells above and below layer 4 are complex glosses over major layer-to-layer differences, because complex cells are far from all alike.
They all have in common the defining characteristic of complex cells—they respond throughout their receptive field to a properly oriented moving line regardless of its exact position—but they differ in other ways. We can distinguish four subtypes that tend to be housed in different layers. In layers 2 and 3, most complex cells respond progressively better the longer the slit (they show length summation), and the response becomes weaker when the line exceeds a critical length only if a cell is end stopped. For cells in layer 5, short slits, covering only a small part of the length of a receptive field, work about as well as long ones; the receptive fields are much larger than the fields of cells in layers 2 and 3. For cells in layer 6, in contrast, the longer an optimally oriented line is, the stronger are the responses, until the line spans the entire length of the field, which is several times greater than the width (the distance over which a moving line evokes responses). The field is thus long and narrow. We can conclude that axons running from layers 5, 6, and 2 and 3 to different targets in the brain (the superior culliculus, geniculate, the other visual cortical areas)
must carry somewhat different kinds of visual information.
In summary, from layer to layer we find differences in the way cells behave that seem more fundamental than differences, say, in optimal orientation or in ocular dominance. The most obvious of these layer-to-layer differences is in response complexity, which reflects the simple anatomical fact that some layers are closer than others to the input.
Eye-dominance groupings of cells in the striate cortex were the first to be recognized, largely because they are rather coarse. Because we now have many methods for examining them, they are now the best-known subdivision. It was obvious soon after the first recordings from monkeys that every time the electrode entered the cortex perpendicular to the surface, cell after cell favored the same eye, as shown in the illustration on this page. If the electrode was pulled out and reinserted at a new site a few millimeters away, one eye would again dominate, perhaps the same eye and perhaps the other one. In layer 4C, which receives the input from the geniculates, the dominant eye seemed to have not merely an advantage, but a monopoly. In the layers above and below, and hence farther along in the succession of synapses, over half of the cells could also be influenced from the nondominant eye—we call these cells binocular.
If instead of placing the electrode perpendicular to the surface, we introduced it obliquely, as close to parallel to the surface as could be managed, the eye dominance alternated back and forth, now one eye dominating and now the other. A complete cycle, from one eye to the other and back, occurred roughly once every millimeter. Obviously, the cortex seen from above must consist of some kind of mosaic composed of left-eye and right-eye regions.
The basis of the eye alternation became clear when new staining methods revealed how single geniculo-cortical axons branch and distribute themselves in the cortex. The branches of a single axon are such that its thousands of terminals form two or three clumps in layer 4C, each 0.5 millimeter wide, separated by o. 5-millimeter gaps, as shown in the illustration of synapse endings on this page. Because geniculate cells are monocular, any individual axon obviously belongs either to the left eye or the right eye. Suppose the green axon in the illustration is a left-eye fiber; it turns out that every left-eye fiber entering the cortex in this region will have its terminal branches in these same 0.5-millimeter clumps. Between the clumps, the 0.5-millimeter gaps are occupied by right-eye terminals. This special distribution ofgeniculo-cortical fibers in layer 4C explains at once the strict monocularity of cells in that layer.
To select one fiber and stain it and only it required a new method, first invented in the late 1970s. It is based on the phenomenon of axon transport.
Materials, either proteins or larger particles, are constantly being transported, in both directions, along the interior of axons, some at rates measured in centimeters per hour, others at rates of about a millimeter per day. To stain a single axon, we inject it through a micropipette with a substance that is known to be transported and that will stain the axon without distorting the cell. The favorite substance at present is an enzyme called horseradish peroxidase. It is transported in both directions, and it catalyzes a chemical reaction that forms the basis of an exceedingly sensitive stain. Because it is a catalyst, minute amounts of it can generate a lot of stain and because it is of plant origin, none of it is normally around to give unwanted background staining.
The microelectrode penetrations in the vertical axis, by showing the cortex subdivided into ocular-dominance columns extending from the surface to the white matter, confirmed anatomical evidence that a patch of cells in layer 4C is the main supplier of visual information to cell layers above and below it. The existence of some horizontal and diagonal connections extending a millimeter or so in all directions must result in some smudging of the left-eye versus right-eye zones in the layers above and below 4C, as shown in the diagram on this page. We can expect that a cell sitting directly above the center of a layer-4 left-eye patch will therefore strongly favor that eye and perhaps be monopolized by it, whereas a cell closer to the border between two patches may be binocular and favor neither eye. Microelectrode penetrations that progress horizontally through one upper cortical layer, or through layer 5 or 6, recording cell after cell, do indeed find a progression of ocular dominance in which cells first favor one eye strongly, then less strongly, are then equally influenced, and then begin to favor the other eye progressively more strongly. This smooth alternation back and forth contrasts sharply with the sudden transitions we find if we advance the electrode through layer 4C.
Viewed from the side, the subdivisions in layer 4 appeared as patches. But we wanted to know how the pattern would appear if we stood above the cortex and looked down. Suppose we have two regions, black and white, on a surface; topologically, we can partition them off in several different ways: in a checkerboard-like mosaic, in a series of black and white stripes, in black islands on a white ocean, or in any combination of these. The figures above show three possible patterns. To tackle the problem with microelectrodes alone amounts to using a one-dimensional technique to answer a three-dimensional question. That can be frustrating, like trying to cut the back lawn with a pair of nail scissors. One would prefer to switch to a completely different type of work, say farming, or the law. (In the early 1960s, when Torsten Weisel and I were more patient and determined, we actually did try to work out the geometry, with some success. And I actually did cut our back lawn once in those days, admittedly with kitchen scissors rather than nail scissors, because we could not afford a lawn mower. We were poorer than modern graduate students, but perhaps more patient.)
The ocular-dominance column borders in upper (2, 3) and lower (5, 6) layers are blurred, compared to the sharp boundaries in layer 4. The arrows illustrate electrode tracks made in layer 4 (upper left) and layer 2 or 3 (upper right). The lower diagrams plot ocular dominance of cells recorded along the tracks. In layer 4, we find abrupt alternation between group i (contralateral eye only) and group 7 (ipsilateral eye only). In other layers, we find binocular cells, and the eye dominance alternates by going through the intermediate degrees of eye preference. (1, 4, and 7 refer to ocular dominance.)
Each geniculate axon ascends through the deep layers of the striate cortex, subdividing repeatedly, finally terminating in 4C in o. 5 millimeter-wide clusters of synaptic endings, separated by blank areas, also 0.5 millimeter wide. All fibers from one eye occupy the same patches: the gaps are occupied by the other eye. The horizontal extent of the patches from a single fiber may be 2 to 3 millimeters for magnocellular terminals in 4Calpha; a parvocellular fiber branches in a more restricted area in 4QBata and generally occupies only one or two patches.
Ocular dominance remains constant in vertical microelectrode penetrations through the striate cortex. Penetrations parallel to the surface show alternation from left eye to right eye and back, roughly one cycle every millimeter.
A rough indication of physiological cell types found in the different layers of the striate cortex.