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This study concerns the transmission of short-wavelength-sensitive (S) cone signals through the primate dorsal lateral geniculate nucleus. The principal cell classes, magnocellular (MC) and parvocellular (PC), are traditionally segregated into on- and off-subtypes on the basis of the sign of their response to luminance variation. Cells dominated by input from S-cones (‘blue-on and blue-off’) are less frequently encountered and their properties are less well understood. Here we characterize the spatial and chromatic properties of a large sample of blue-on and blue-off neurons and contrast them with those of PC and MC neurons. The results confirm that blue-on and blue-off cells have larger receptive fields than PC and MC neurons at equivalent eccentricities. Relative to blue-on cells, blue-off cells are less sensitive to S-cone contrast, have larger receptive fields, and show more low-pass spatial frequency tuning. Thus, blue-on and blue-off neurons lack the functional symmetry characteristic of on- and off-subtypes in the MC and PC pathways. The majority of MC and PC cells received no detectible input from S-cones. Where present, input from S-cones tended to provide weak inhibition to PC cells. All cell types showed evidence of a suppressive extra-classical receptive field driven largely or exclusively by ML-cones. These data indicate that S-cone signals are isolated to supply the classical receptive field mechanisms of blue-on and blue-off cells in the LGN, and that the low spatial precision of S-cone vision has origins in both classical and extraclassical receptive field properties of subcortical pathways.