Eye, Brain, and Vision
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A very oblique penetration through area 17 in a macaque monkey reveals the regular shift in orientation preference of 23 neighboring cells.

ocular-dominance columns. You see the result in the photographs above.
In a very pretty extension of the same idea, Roger Tootell, in Russel De Valois's laboratory at Berkeley, had an animal look with one eye at a large pattern of concentric circles and rays, shown in the top image of the figure on the next page. The resulting pattern on the cortex contains the circles and rays, distorted just as expected by the variations in magnification (the distance on the cortex corresponding to i degree of visual field), a phenomenon related to the change in visual acuity between the fovea and periphery of the eye. Over and above that, each circle or ray is broken up by the fine ocular-dominance stripes. Stimulating both eyes would have resulted in continuous bands. Seldom can we illustrate so many separate facts so neatly, all in a single experiment.
Cats, several kinds of monkeys, chimpanzees, and man all possess oculardominance columns. The columns are absent in rodents and tree shrews; and although hints of their presence can be detected physiologically in the squirrel monkey, a new world monkey, present anatomical methods do not reveal the columns. At present we don't know what purpose this highly patterned segregation of eye influence serves, but one guess is that it has something to do with stereopsis (see Chapter 7).
Subdivisions of the cortex by specialization in cell function have been found in many regions besides the striate cortex. They were first seen in the somatosensory cortex by Vernon Mountcastle in the mid-1950s, in what was surely the most important set of observations on cortex since localization of function was first discovered. The somatosensory is to touch, pressure, and joint position what the striate cortex is to vision. Mountcastle showed that this cortex is similarly subdivided vertically into regions in which cells are sensitive to touch and regions in which cells respond to bending of joints or applying deep pressure to a limb. Like ocular-dominance columns, the regions are about half a millimeter across, but whether they form stripes, a checkerboard, or an oceanand-islands pattern is still not clear. The term column was coined by Mountcastie, so one can probably assume that he had a pillarlike structure in mind. We now know that the word slab would be more suitable for the visual cortex.
Terminology is hard to change, however, and it seems best to stick to the well-known term, despite its shortcomings. Today we speak of columnar subdivisions when some cell attribute remains constant from surface to white matter and varies in records taken parallel to the surface. For reasons that will become clear in the next chapter, we usually restrict the concept to exclude the topographic representation, that is, position of receptive fields on the retina or position on the body.



                               ORIENTATION COLUMNS
In the earliest recordings from the striate cortex, it was noticed that whenever two cells were recorded together, they agreed not only in their eye preference, but also in their preferred orientation. You might reasonably ask at this point whether next-door neighboring cells agree in all their properties: the answer is clearly no. As I have mentioned, receptive-field positions are usually not quite the same, although they usually overlap; directional preferences are often opposite, or one cell may show a marked directional preference and the other show none. In layers 2 and 3, where end-stopping is found, one cell may show no stopping when its neighbor is completely stopped. In contrast, it is very rare for two cells recorded together to have opposite eye preference or any obvious difference in orientation.
Orientation, like eye preference, remains constant in vertical penetrations through the full cortical thickness. In layer 4C Bata, as described earlier, cells show no orientation preference at all, but as soon as we reach layer 5, the cells show strong orientation preference and the preferred orientation is the same as it was above layer 4C. If we pull out the electrode and reinsert it somewhere else, the whole sequence of events is seen again, but a different orientation very likely will prevail. The cortex is thus subdivided into slender regions of constant orientation, extending from surface to white matter but interrupted by layer 4, where cells have no orientation preference.
If, on the other hand, the electrode is pushed through the cortex in a direction parallel to the surface, an amazingly regular sequence of changes in orientation occurs: every time the electrode advances 0.05 millimeter (50 micrometers), on the average the preferred orientation shifts about 10 degrees clockwise or counterclockwise. Consequently a traverse of i millimeter typically records a total shift of 180 degrees. Fifty micrometers and 10 degrees are close to the present limits of the precision of measurements, so that it is impossible to say whether orientation varies in any sense continuously with electrode position, or shifts in discrete steps.


















In the two figures on this page, a typical experiment is illustrated for part of a close-to-horizontal penetration through area 17, in which 23 cells were recorded. The eyes were not perfectly aligned on the screen (because of the anesthetic and a muscle-relaxing agent), so that the projections of the foveas of the two eyes were separated by about 2 degrees. The color circles in the figure above represent roughly the sizes of the receptive fields, about a degree in diameter, positioned 4 degrees below and to the left of the foveal projections—the records were from the right hemisphere. The first cell, 96, was binocular, but the next 14 were dominated strongly by the right eye.
From then on, for cells in to 118, the left eye took over. You can see how regularly the orientations were shifting during this sequence, in this case always counterclockwise. When the shift in orientation is plotted against track distance (in the graph on the next page), the points form an almost perfect straight line. The change from one eye to the other was not accompanied by any obvious change either in the tendency to shift counterclockwise or in the slope of the line. We interpret this to mean that the two systems of groupings, by eye dominance and by orientation, are not closely related. It is as though the cortex were diced up in two completely different ways.
In such penetrations, the direction of orientation shifts may be clockwise or counterclockwise, and most penetrations, if long enough, sooner or later show shifts in the direction of rotation; these occur at unpredictable intervals of a

   
 

The results of the experiment shown on the facing page are plotted in degrees, against the distance the electrode had traveled. (Because the electrode was so slanted that it was almost parallel to the cortical surface, the track distance is almost the same as the distance along the surface.) In this experiment 180 degrees, a full rotation, corresponded to about 0.7 millimeter.
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In this experiment by Roger Tootell, the target-shaped stimulus with radial lines was centered on an anesthetized macaque monkey's right visual field for 45 minutes after injection with radioactive 2-deoxyglucose.
One eye was held closed. The lower picture shows the labeling in the striate cortex of the left hemisphere. This autoradiograph shows a section parallel to the surface; the cortex was flattened and frozen before sectioning. The roughly vertical lines of label represent the (semi)circular stimulus lines;
the horizontal lines of label represent the radial lines in the right visual field. The hatching within each line of label is caused by only one eye having been stimulated and represents ocular-dominance columns.


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Two experiments using radioactive deoxyglucose. Top: A cross section of the two hemispheres through the occipital lobes in a control animal that had its visual field stimulated with both eyes open following the intravenous injection. Bottom: After injection, an animal viewed the stimulus with one eye open and the other closed. The ocular-dominance patterns are clearly visible in the cortex. This experiment was done by C. Kennedy, M. H. Des Rosiers, 0. Sakurada, M. Shinohara, M. Reivich, J. W. Jehle, and L. Sokoloff.