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

2021; Elsevier BV; Volume: 31; Issue: 15 Linguagem: Inglês

10.1016/j.cub.2021.05.024

1879-0445

Joshua W. Mouland, Abigail Pienaar, Christopher Williams, Alex J. Watson, Robert J. Lucas, Timothy M. Brown,

Retinal Development and Disorders

Color vision, originating with opponent processing of spectrally distinct photoreceptor signals, plays important roles in animal behavior.1Price T.D. Sensory drive, color, and color vision.Am. Nat. 2017; 190: 157-170Crossref PubMed Scopus (32) Google Scholar, 2Spitschan M. Lucas R.J. Brown T.M. Chromatic clocks: color opponency in non-image-forming visual function.Neurosci. Biobehav. Rev. 2017; 78: 24-33Crossref PubMed Scopus (23) Google Scholar, 3Baden T. Osorio D. The retinal basis of vertebrate color vision.Annu. Rev. Vis. Sci. 2019; 5: 177-200Crossref PubMed Scopus (24) Google Scholar, 4Thoreson W.B. Dacey D.M. Diverse cell types, circuits, and mechanisms for color vision in the vertebrate retina.Physiol. Rev. 2019; 99: 1527-1573Crossref PubMed Scopus (35) Google Scholar 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.5Applebury M.L. Antoch M.P. Baxter L.C. Chun L.L. Falk J.D. Farhangfar F. Kage K. Krzystolik M.G. Lyass L.A. Robbins J.T. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning.Neuron. 2000; 27: 513-523Abstract Full Text Full Text PDF PubMed Google Scholar, 6Baden T. Schubert T. Chang L. Wei T. Zaichuk M. Wissinger B. Euler T. A tale of two retinal domains: near-optimal sampling of achromatic contrasts in natural scenes through asymmetric photoreceptor distribution.Neuron. 2013; 80: 1206-1217Abstract Full Text Full Text PDF PubMed Google Scholar, 7Nadal-Nicolás F.M. Kunze V.P. Ball J.M. Peng B.T. Krishnan A. Zhou G. Dong L. Li W. True S-cones are concentrated in the ventral mouse retina and wired for color detection in the upper visual field.eLife. 2020; 9: e56840Crossref PubMed Scopus (23) Google Scholar, 8Haverkamp S. Wässle H. Duebel J. Kuner T. Augustine G.J. Feng G. Euler T. The primordial, blue-cone color system of the mouse retina.J. Neurosci. 2005; 25: 5438-5445Crossref PubMed Scopus (203) Google Scholar However, recent data indicate that mice exhibit robust chromatic discrimination within the central-upper visual field.9Denman D.J. Luviano J.A. Ollerenshaw D.R. Cross S. Williams D. Buice M.A. Olsen S.R. Reid R.C. Mouse color and wavelength-specific luminance contrast sensitivity are non-uniform across visual space.eLife. 2018; 7: e31209Crossref PubMed Scopus (31) Google Scholar 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.10Chang L. Breuninger T. Euler T. Chromatic coding from cone-type unselective circuits in the mouse retina.Neuron. 2013; 77: 559-571Abstract Full Text Full Text PDF PubMed Scopus (56) Google Scholar, 11Joesch M. Meister M. A neuronal circuit for colour vision based on rod-cone opponency.Nature. 2016; 532: 236-239Crossref PubMed Google Scholar, 12Stabio M.E. Sabbah S. Quattrochi L.E. Ilardi M.C. Fogerson P.M. Leyrer M.L. Kim M.T. Kim I. Schiel M. Renna J.M. et al.The M5 cell: a color-opponent intrinsically photosensitive retinal ganglion cell.Neuron. 2018; 97: 150-163.e4Abstract Full Text Full Text PDF PubMed Scopus (36) Google Scholar, 13Szatko K.P. Korympidou M.M. Ran Y. Berens P. Dalkara D. Schubert T. Euler T. Franke K. Neural circuits in the mouse retina support color vision in the upper visual field.Nat. Commun. 2020; 11: 3481Crossref PubMed Scopus (17) Google Scholar 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.