Colour vision, originating with opponent processing of spectrally distinct photoreceptor signals, plays important roles in animal behaviour1-4. Surprisingly, however, comparatively little is understood about colour processing in the brain, including in widely used laboratory mammals such as mice. The retinal gradient in S- and M-cone opsin (co-)expression has traditionally been considered an impediment to mouse colour vision5-8. However, recent data indicate that mice exhibit robust chromatic discrimination within the central-upper visual field9. Retinal colour-opponency has been reported to emerge from superimposing inhibitory surround receptive fields on the cone opsin expression gradient, and by introducing opponent rod-signals in retinal regions with sparse M-cone opsin expression10-13. The relative importance of these proposed mechanisms in determining the properties of neurons at higher visual processing stages remains unknown. We address these questions using multielectrode recordings from the lateral geniculate nucleus (LGN) in mice with altered M-cone spectral sensitivity (Opn1mwR) and multispectral stimuli that allow selective modulation of signalling by individual opsin classes. Remarkably, we find many (~25%) LGN cells are colour-opponent, that such cells are localised to a distinct medial LGN zone and that their properties cannot simply be explained by the proposed retinal opponent mechanisms. Opponent responses in LGN can be driven solely by cones, independent of cone-opsin expression gradients and rod input, with many cells exhibiting spatially congruent antagonistic receptive fields. Our data therefore suggest previously unidentified mechanisms may support extensive and sophisticated colour processing in the mouse LGN.