The organization of chromatic and spatial interactions in the primate striate cortex

Abstract

The cytochrome oxidase-rich patches or blobs of the monkey striate cortex have been shown to contain cells that have unoriented receptive fields, many of which are color selective. We studied the functional organization of color opponency in the blob regions of the parafoveal representation of the visual cortex. We also examined the patterns of connectivity among blob and nonblob cells by multiple electrode penetrations and cross-correlation analysis. Some of the color-selective cells in the blobs exhibited receptive fields that were similar to those found in the parvocellular layers of the lateral geniculate nucleus (LGN): one type exhibited center-surround spatial and chromatic opponency corresponding to the Type I cell found in the LGN; another had center-only chromatic opponency, corresponding to the Type II cell of the LGN. A blob color-selective cell with no LGN counterpart had center color opponency with a nonchromatically opponent surround antagonism. We termed this cell the 'modified Type II' cell. Contrary to previous reports, few true double color-opponent cells were found. Some blob cells previously characterized as double opponent probably belong to our modified Type II category and, unlike true double opponent cells, do not respond well to isoluminant color boundaries. Occasional color-selective oriented cells were either intermixed or in close proximity to blob cells. Neighboring electrode penetrations within the same blob yielded cells of the same color opponency, either red versus green or blue versus yellow, suggesting that individual blobs are dedicated to processing one color opponency. Blobs dedicated to red/green color opponency were 3 times more numerous than blue/yellow blobs. Furthermore, the cells in layer 4C lying beneath blobs of a given color opponency had identical color opponency to the overlying cells in blobs. Cross-correlation analysis of pairs of nonblob, oriented cells in the superficial layers showed interactions between cells with matched orientation and eye preference, at varying horizontal separations. Such interactions are consistent with anatomically demonstrated clustered horizontal connections. Positive cross-correlograms were found between blob cells in the same and in adjacent blobs when the cells' receptive field type, color opponency, and ocular dominance matched. Correlograms also indicated monosynaptic connections from Type II to modified Type II cells of the same color opponency, suggesting that Type II cells may contribute to the construction of the modified Type II fields in the cortex. Finally, correlograms indicated that color-oriented cells receive synaptic input from Type I and modified Type II cells.