Anatomical demonstration of columns in the monkey striate cortex.
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Biomedical subjects
Publications and source records attributed to D H Hubel.
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On anatomical and physiological grounds a zone of cat cortex deep in the medial bank of the suprasylvian sulcus (the Clare-Bishop area) is known to receive strong visual projections both from the lateral geniculate body and area 17. We have mapped receptive fields of single cells in this area in eight cats. Active responses to visual stimuli were found over most of the medial bank of the suprasylvian sulcus extending to the depths and over to the lowest part of the lateral bank. The area is clearly topographically arranged. The first responsive cells, recorded over the lateral convexity and 2-3 mm down the medial bank, had receptive fields in the far periphery of the contralateral visual fields. The receptive fields tended to be large, but showed considerable variation in size and scatter in their positions. As the electrode advanced down the bank, fields of successively recorded cells gradually tended to move inwards, so that in the depths of the sulcus the inner borders of many of the fields reached the vertical mid line. Here the fields were smaller, though they still varied very much in size. Receptive fields were larger than in 17, 18, or 19, but otherwise were not obviously different from the complex and lower-order hypercomplex fields in those areas. No simple fields, or concentric fields of the retino-geniculate type, were seen. Cells with common receptive-field orientation were grouped together, but whether or not the grouping occurs in columns was not established. Most cells were driven independently by the two eyes. Fields in the two eyes seemed to be identical in organization. Cells dominated by the contralateral eye were much more common than ipsilaterally dominated ones, but when cells with parafoveal and peripheral fields were considered separately, the asymmetry was seen to apply mainly to cells with peripheral fields.
1. The striate cortex was studied in lightly anaesthetized macaque and spider monkeys by recording extracellularly from single units and stimulating the retinas with spots or patterns of light. Most cells can be categorized as simple, complex, or hypercomplex, with response properties very similar to those previously described in the cat. On the average, however, receptive fields are smaller, and there is a greater sensitivity to changes in stimulus orientation. A small proportion of the cells are colour coded.2. Evidence is presented for at least two independent systems of columns extending vertically from surface to white matter. Columns of the first type contain cells with common receptive-field orientations. They are similar to the orientation columns described in the cat, but are probably smaller in cross-sectional area. In the second system cells are aggregated into columns according to eye preference. The ocular dominance columns are larger than the orientation columns, and the two sets of boundaries seem to be independent.3. There is a tendency for cells to be grouped according to symmetry of responses to movement; in some regions the cells respond equally well to the two opposite directions of movement of a line, but other regions contain a mixture of cells favouring one direction and cells favouring the other.4. A horizontal organization corresponding to the cortical layering can also be discerned. The upper layers (II and the upper two-thirds of III) contain complex and hypercomplex cells, but simple cells are virtually absent. The cells are mostly binocularly driven. Simple cells are found deep in layer III, and in IV A and IV B. In layer IV B they form a large proportion of the population, whereas complex cells are rare. In layers IV A and IV B one finds units lacking orientation specificity; it is not clear whether these are cell bodies or axons of geniculate cells. In layer IV most cells are driven by one eye only; this layer consists of a mosaic with cells of some regions responding to one eye only, those of other regions responding to the other eye. Layers V and VI contain mostly complex and hypercomplex cells, binocularly driven.5. The cortex is seen as a system organized vertically and horizontally in entirely different ways. In the vertical system (in which cells lying along a vertical line in the cortex have common features) stimulus dimensions such as retinal position, line orientation, ocular dominance, and perhaps directionality of movement, are mapped in sets of superimposed but independent mosaics. The horizontal system segregates cells in layers by hierarchical orders, the lowest orders (simple cells monocularly driven) located in and near layer IV, the higher orders in the upper and lower layers.
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Human vision has the remarkable property that, over a wide range, changes in the wavelength composition of the source light illuminating a scene result in very little change in the colour of any of the objects. This colour constancy can be explained by the retinex theory, which predicts the colour of a point on any object from a computed relationship between the radiation from that point and the radiation from all the other points in the field of view (Fig. 1). Thus the computations for colour perception occur across large distances in the visual field. It has not been clear, however, whether these long-range interactions take place in the retina or the cortex. Reports that long-range colour interactions can be reproduced binocularly when one band of wavelengths enters one eye and a different band enters the other might seem to establish the cortex as the site of the computation. Many observers, however, see very unsatisfactory colour or no colour at all in this binocular situation, suggesting that the cortex may not be the only site at which the computation is carried out, or even the most important site. We have now tested the role of the cortex in a human subject in whom the nerve fibres connecting cortical areas subserving two separate parts of the visual field had been severed, and find that the cortex is necessary for long-range colour computations.
When the primate primary visual cortex, area 17, is stained for the mitochondrial enzyme cytochrome oxidase, it shows a striking polka-dot pattern (cytochrome oxidase blobs). Area 18, the second visual area, shows a cytochrome-oxidase pattern of coarse alternating thick and thin stripes running perpendicular to the 17-18 border and separated by lighter (interstripe) regions. Here we show that the thin cytochrome oxidase stripes, and possibly also the thick stripes, in area 18 receive projections specifically from the blobs in area 17, and that the interstripe regions of 18 receive projections from the interblob matrix of area 17. This indicates a specificity of cortico-cortical connections far exceeding the demands of topographical mapping. Together with our physiological results, it suggests that within the pathway from area 17 to area 18 different kinds of information may be handled separately and in parallel.
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In primates, both the primary and secondary visual cortical areas can be subdivided histologically by staining for the mitochondrial enzyme cytochrome oxidase. In the primary visual cortex (area 17, the first cortical receiving area for visual information) these histological differences correspond to functional subdivisions, cytochrome-dark regions being concerned with information about colour and cytochrome-light regions concerned with form. Here we report that the second visual area, area 18, which receives its main cortical input from area 17 (refs 7,8), similarly has functional subdivisions that correspond to the cytochrome oxidase staining pattern. In area 18 the segregation between form and colour is maintained, reinforcing our notion that form and colour information follow parallel pathways. The specific differences between cells in areas 17 and 18 suggest that a possible step in hierarchical information processing is spatial generalization, analogous to the difference between simple and complex cells.
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