Extensive cone-dependent spectral opponency within a discrete zone of the lateral geniculate nucleus supporting mouse color vision

Color vision, originating with opponent processing of spectrally distinct photoreceptor signals, plays important roles in animal behavior.1–4 Surprisingly, however, comparatively little is understood about color 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 color vision.5–8 However, recent data indicate that mice exhibit robust chromatic discrimination within the central-upper visual field.9 Retinal color 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 expression.10–13 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 signaling by individual opsin classes. Remarkably, we find many (∼25%) LGN cells are color opponent, that such cells are localized 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 color processing in the mouse LGN. •Color opponency is common among neurons within a chromatic zone in the mouse LGN•Cone inputs to LGN drive color opponency across mesopic to photopic light levels•Cone inputs to opponent neurons derive from central and upper visual field•Subsets of LGN neurons display opponency for small or large stimuli only Mouland et al. examine color processing in the mouse visual thalamus. They show that color opponency is widespread among cells within a specific zone of the lateral geniculate nucleus and that cones drive such responses, independent of cone-opsin expression gradients and rod input, providing a robust capacity for color discrimination in mice.