The signals of cone photoreceptors are transmitted from retina to cortex through the lateral geniculate nucleus (LGN), by a small number of distinct cone-opponent pathways. The weights that these pathways attach to cone inputs, and how their signals are combined in cortex, remain controversial. Two of the pathways are fairly well established: one opposes the signals of L- and M-cones (L-M), and one opposes excitatory signals from S-cones to inhibitory signals from L- and M-cones (S-on). In extracellular recordings from macaque LGN we first show that a third pathway, in which neurons get inhibitory input from S-cones (S-off), is functionally distinct: these neurons are less sensitive to S-cone modulation than S-on neurons; they oppose the signals of L-cones to those of S- and M-cones; unlike S-on and L-M neurons they are desensitized by prolonged exposure to chromatic modulation (contrast adaptation). We then show that in visual cortex (V1) these pathways are combined in an approximately linear manner, producing among colour-preferring neurons a wide variety of chromatic signatures. The LGN pathways are also combined non-linearly in V1 to form regulatory gain controls, which help make the chromatic tuning of neurons largely independent of the prevailing level of contrast. Both the linear receptive field and the gain controls in V1 can be desensitized by prolonged exposure to chromatic modulation. This is presumably important in the representation of suprathreshold colours during natural viewing.