{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"institution":[{"name":"bioRxiv"}],"indexed":{"date-parts":[[2026,1,23]],"date-time":"2026-01-23T09:19:42Z","timestamp":1769159982886,"version":"3.49.0"},"posted":{"date-parts":[[2023,9,16]]},"group-title":"Neuroscience","reference-count":99,"publisher":"openRxiv","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"accepted":{"date-parts":[[2023,9,16]]},"abstract":"<jats:p>A long-standing question in vision science is how the three cone photoreceptor types \u2013 long (L), medium (M) and short (S) wavelength sensitive \u2013 combine to generate our perception of color. Hue perception can be described along two opponent axes: red-green and blue-yellow. Psychophysical measurements of color appearance indicate that the cone inputs to the red-green and blue-yellow opponent axes are M vs. L+S and L vs. M+S, respectively. However, the \u201ccardinal directions of color space\u201d revealed by psychophysical measurements of color detection thresholds are L vs. M and S vs. L+M. The cardinal directions match the most common cone-opponent retinal ganglion cells (RGCs) in the primate retina. Accordingly, the cone opponency necessary for color appearance is thought to be established in cortex. However, small populations with the appropriate M vs. L+S and L vs. M+S cone-opponency have been reported in large surveys of cone inputs to primate RGCs and their projections to the lateral geniculate nucleus (LGN) yet their existence continues to be debated. Resolving this long-standing open question is needed as a complete account of the cone-opponency in the retinal output is critical for efforts to understand how downstream neural circuits process color. Here, we performed adaptive optics calcium imaging to longitudinally and noninvasively measurements of the foveal RGC light responses in the living macaque eye. We confirm the presence of L vs. M+S and M vs. L+S neurons with non-cardinal cone-opponency and demonstrate that cone-opponent signals in the retinal output are substantially more diverse than classically thought.<\/jats:p>","DOI":"10.1101\/2023.09.15.557995","type":"posted-content","created":{"date-parts":[[2023,9,16]],"date-time":"2023-09-16T23:00:11Z","timestamp":1694905211000},"source":"Crossref","is-referenced-by-count":3,"title":["Cone-Opponent Ganglion Cells in the Primate Fovea Tuned to Non-Cardinal Color Directions"],"prefix":"10.64898","author":[{"given":"Tyler","family":"Godat","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kendall","family":"Kohout","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qiang","family":"Yang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Keith","family":"Parkins","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Juliette E.","family":"McGregor","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"William H.","family":"Merigan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David R.","family":"Williams","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sara S.","family":"Patterson","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"54368","reference":[{"key":"2023092005300569000_2023.09.15.557995v1.1","doi-asserted-by":"publisher","DOI":"10.1002\/cne.903430306"},{"key":"2023092005300569000_2023.09.15.557995v1.2","doi-asserted-by":"publisher","DOI":"10.1162\/neco.1992.4.4.559"},{"key":"2023092005300569000_2023.09.15.557995v1.3","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(93)90065-5"},{"key":"2023092005300569000_2023.09.15.557995v1.4","unstructured":"Barlow H (1961) Possible principles underlying the transformations of sensory messages. In: Sensory Communication ( Rosenbith WA , ed), pp 217\u2013234. Cambridge, MA: MIT Press."},{"key":"2023092005300569000_2023.09.15.557995v1.5","doi-asserted-by":"crossref","first-page":"2560","DOI":"10.1364\/AO.12.002560","article-title":"Maxwellian View stimulator for electrophysiological or psychophysical work","volume":"12","year":"1973","journal-title":"Appl Opt"},{"key":"2023092005300569000_2023.09.15.557995v1.6","doi-asserted-by":"publisher","DOI":"10.7554\/elife.39324"},{"key":"2023092005300569000_2023.09.15.557995v1.7","doi-asserted-by":"publisher","DOI":"10.1002\/col.5080050104"},{"key":"2023092005300569000_2023.09.15.557995v1.8","unstructured":"Brainard DH (1996) Cone contrast and opponent modulation color spaces. In: Human Color Vision ( Kaiser PK , Boynton RM , eds), pp 563\u2013579. Washington, DC: Optical Society of America."},{"key":"2023092005300569000_2023.09.15.557995v1.9","doi-asserted-by":"publisher","DOI":"10.1163\/156856897X00357"},{"key":"2023092005300569000_2023.09.15.557995v1.10","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.1983.0090"},{"key":"2023092005300569000_2023.09.15.557995v1.11","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.3237-06.2006"},{"key":"2023092005300569000_2023.09.15.557995v1.12","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1364\/JOSAA.17.000597","article-title":"Representation of cone signals in the primate retina","volume":"17","year":"2000","journal-title":"J Opt Soc Am A"},{"key":"2023092005300569000_2023.09.15.557995v1.13","doi-asserted-by":"publisher","DOI":"10.1038\/381613a0"},{"key":"2023092005300569000_2023.09.15.557995v1.14","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(00)80846-6"},{"key":"2023092005300569000_2023.09.15.557995v1.15","doi-asserted-by":"publisher","DOI":"10.1038\/nature02167"},{"key":"2023092005300569000_2023.09.15.557995v1.16","doi-asserted-by":"publisher","DOI":"10.1038\/nature12354"},{"key":"2023092005300569000_2023.09.15.557995v1.17","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.21-08-02768.2001"},{"key":"2023092005300569000_2023.09.15.557995v1.18","doi-asserted-by":"crossref","unstructured":"Conway BR , Malik-Moraleda S , Gibson E (2023) Color appearance and the end of Hering\u2019s Opponent-Colors Theory. Trends Cogn Sci:1\u201314.","DOI":"10.1016\/j.tics.2023.06.003"},{"key":"2023092005300569000_2023.09.15.557995v1.19","doi-asserted-by":"publisher","DOI":"10.1002\/cne.903000103"},{"key":"2023092005300569000_2023.09.15.557995v1.20","first-page":"1080","article-title":"Morphology of a small-field bistratified ganglion cell type in the macaque and human retina","volume":"10","year":"1993","journal-title":"Vis Neurosci"},{"key":"2023092005300569000_2023.09.15.557995v1.21","doi-asserted-by":"publisher","DOI":"10.1016\/S0959-4388(03)00103-X"},{"key":"2023092005300569000_2023.09.15.557995v1.22","doi-asserted-by":"publisher","DOI":"10.1364\/JOSAA.29.00A157"},{"key":"2023092005300569000_2023.09.15.557995v1.23","doi-asserted-by":"publisher","DOI":"10.1016\/j.visres.2012.04.006"},{"key":"2023092005300569000_2023.09.15.557995v1.24","first-page":"441","article-title":"Signals from blue cones in \u201cred-green\u201d opponent-color ganglion cells of the macaque retina","volume":"19","year":"1978","journal-title":"Vision Res"},{"key":"2023092005300569000_2023.09.15.557995v1.25","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.1975.sp011086"},{"key":"2023092005300569000_2023.09.15.557995v1.26","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.1975.sp011087"},{"key":"2023092005300569000_2023.09.15.557995v1.27","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(74)90116-3"},{"key":"2023092005300569000_2023.09.15.557995v1.28","doi-asserted-by":"crossref","unstructured":"De Valois RL (2004a) The neural coding of color. In: The New Visual Neurosciences ( Werner JS , Chalupa LM , eds), pp 1003\u20131013. MIT Press.","DOI":"10.7551\/mitpress\/7131.003.0075"},{"key":"2023092005300569000_2023.09.15.557995v1.29","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(93)90240-W"},{"key":"2023092005300569000_2023.09.15.557995v1.30","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.1984.sp015499"},{"key":"2023092005300569000_2023.09.15.557995v1.31","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.1984.sp015498"},{"key":"2023092005300569000_2023.09.15.557995v1.32","doi-asserted-by":"publisher","DOI":"10.1016\/j.visres.2009.07.005"},{"key":"2023092005300569000_2023.09.15.557995v1.33","doi-asserted-by":"publisher","DOI":"10.1038\/nature09424"},{"key":"2023092005300569000_2023.09.15.557995v1.34","doi-asserted-by":"publisher","DOI":"10.3758\/BF03207340"},{"key":"2023092005300569000_2023.09.15.557995v1.35","doi-asserted-by":"publisher","DOI":"10.1167\/14.1.1"},{"key":"2023092005300569000_2023.09.15.557995v1.36","doi-asserted-by":"publisher","DOI":"10.1016\/S0166-2236(96)10036-9"},{"key":"2023092005300569000_2023.09.15.557995v1.37","doi-asserted-by":"publisher","DOI":"10.1167\/18.4.18"},{"key":"2023092005300569000_2023.09.15.557995v1.38","doi-asserted-by":"crossref","first-page":"e0278261","DOI":"10.1371\/journal.pone.0278261","article-title":"In vivo chromatic and spatial tuning of foveolar retinal ganglion cells in Macaca fascicularis","volume":"17","year":"2022","journal-title":"PLoS ONE"},{"key":"2023092005300569000_2023.09.15.557995v1.39","doi-asserted-by":"publisher","DOI":"10.1016\/J.Neuron.2009.12.009"},{"key":"2023092005300569000_2023.09.15.557995v1.40","doi-asserted-by":"publisher","DOI":"10.1364\/OE.14.007144"},{"key":"2023092005300569000_2023.09.15.557995v1.41","doi-asserted-by":"publisher","DOI":"10.1016\/j.neuroscience.2014.10.007"},{"key":"2023092005300569000_2023.09.15.557995v1.42","doi-asserted-by":"crossref","first-page":"287","DOI":"10.1146\/annurev-vision-121219-081801","article-title":"Signals related to color in the early visual cortex","volume":"6","year":"2020","journal-title":"Annu Rev Vis Sci"},{"key":"2023092005300569000_2023.09.15.557995v1.43","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(77)90014-1"},{"key":"2023092005300569000_2023.09.15.557995v1.44","doi-asserted-by":"publisher","DOI":"10.1167\/19.4.13"},{"key":"2023092005300569000_2023.09.15.557995v1.45","doi-asserted-by":"crossref","first-page":"e2300545120","DOI":"10.1073\/pnas.2300545120","article-title":"Comparative connectomics reveals noncanonical wiring for color vision in human foveal retina","volume":"120","year":"2023","journal-title":"Proc Natl Acad Sci"},{"key":"2023092005300569000_2023.09.15.557995v1.46","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.23-30-09881.2003"},{"key":"2023092005300569000_2023.09.15.557995v1.47","doi-asserted-by":"publisher","DOI":"10.1038\/348328a0"},{"key":"2023092005300569000_2023.09.15.557995v1.48","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(82)90077-3"},{"key":"2023092005300569000_2023.09.15.557995v1.49","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(86)90068-4"},{"key":"2023092005300569000_2023.09.15.557995v1.50","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.visres.2017.05.013","article-title":"The spatial structure of cone-opponent receptive fields in macaque retina","volume":"151","year":"2018","journal-title":"Vision Res"},{"key":"2023092005300569000_2023.09.15.557995v1.51","first-page":"333","article-title":"Mechanisms of color vision","volume":"3","year":"1988","journal-title":"Crit Rev Neurobiol"},{"key":"2023092005300569000_2023.09.15.557995v1.52","doi-asserted-by":"crossref","unstructured":"Lennie P , Haake PW , Williams DR (1991) The design of chromatically opponent receptive fields. In: Computational Models of Visual Processing ( Landy MS , Movshon JA , eds), pp 71\u201382.Cambridge, MA: MIT Press.","DOI":"10.7551\/mitpress\/2002.003.0010"},{"key":"2023092005300569000_2023.09.15.557995v1.53","doi-asserted-by":"publisher","DOI":"10.1016\/S0042-6989(96)00152-6"},{"key":"2023092005300569000_2023.09.15.557995v1.54","doi-asserted-by":"crossref","unstructured":"Li P , Garg AK , Zhang LA , Rashid MS , Callaway EM (2022) Cone opponent functional domains in primary visual cortex combine signals for color appearance mechanisms.Nat Commun 13.","DOI":"10.1038\/s41467-022-34020-2"},{"key":"2023092005300569000_2023.09.15.557995v1.55","doi-asserted-by":"publisher","DOI":"10.1364\/JOSAA.14.002873"},{"key":"2023092005300569000_2023.09.15.557995v1.56","doi-asserted-by":"crossref","first-page":"108154","DOI":"10.1016\/j.visres.2022.108154","article-title":"Contribution of parasol-magnocellular pathway ganglion cells to foveal retina in macaque monkey","volume":"202","year":"2023","journal-title":"Vision Res"},{"key":"2023092005300569000_2023.09.15.557995v1.57","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2007.05.040"},{"key":"2023092005300569000_2023.09.15.557995v1.58","first-page":"4381","article-title":"The narrow thorny is an S-ON\/S-OFF ganglion cell in the primate retina","volume":"64","year":"2023","journal-title":"Investig Ophthalmol Vis Sci"},{"key":"2023092005300569000_2023.09.15.557995v1.59","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-15317-6"},{"key":"2023092005300569000_2023.09.15.557995v1.60","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0207102"},{"key":"2023092005300569000_2023.09.15.557995v1.61","doi-asserted-by":"publisher","DOI":"10.1038\/eye.2016.257"},{"key":"2023092005300569000_2023.09.15.557995v1.62","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.4738-09.2010"},{"key":"2023092005300569000_2023.09.15.557995v1.63","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(75)90311-9"},{"key":"2023092005300569000_2023.09.15.557995v1.64","doi-asserted-by":"crossref","first-page":"2529","DOI":"10.1016\/j.cub.2022.04.056","article-title":"Conserved circuits for direction selectivity in the primate retina","volume":"32","year":"2022","journal-title":"Curr Biol"},{"key":"2023092005300569000_2023.09.15.557995v1.65","doi-asserted-by":"crossref","first-page":"11913","DOI":"10.1038\/s41598-019-48042-2","article-title":"An S-cone circuit for edge detection in the primate retina","volume":"9","year":"2019","journal-title":"Sci Rep"},{"key":"2023092005300569000_2023.09.15.557995v1.66","doi-asserted-by":"crossref","first-page":"1269","DOI":"10.1016\/j.cub.2020.01.040","article-title":"A color vision circuit for non-image-forming vision in the primate retina","volume":"30","year":"2020","journal-title":"Curr Biol"},{"key":"2023092005300569000_2023.09.15.557995v1.67","doi-asserted-by":"crossref","first-page":"R1409","DOI":"10.1016\/j.cub.2020.10.010","article-title":"Another Blue-ON ganglion cell in the primate retina","volume":"30","year":"2020","journal-title":"Curr Biol"},{"key":"2023092005300569000_2023.09.15.557995v1.68","doi-asserted-by":"publisher","DOI":"10.1016\/0306-4522(88)90020-6"},{"key":"2023092005300569000_2023.09.15.557995v1.69","doi-asserted-by":"publisher","DOI":"10.1068\/p150705"},{"key":"2023092005300569000_2023.09.15.557995v1.70","doi-asserted-by":"crossref","first-page":"e0246952","DOI":"10.1371\/journal.pone.0246952","article-title":"Visual properties of human retinal ganglion cells","volume":"16","year":"2021","journal-title":"PLoS ONE"},{"key":"2023092005300569000_2023.09.15.557995v1.71","first-page":"A1","article-title":"From cones to color vision: a neurobiological model that explains the unique hues","volume":"40","year":"2023","journal-title":"J Opt Soc Am A"},{"key":"2023092005300569000_2023.09.15.557995v1.72","doi-asserted-by":"crossref","unstructured":"Rodieck R (1991) Which cells code for color? In: From Pigments to Perception: Advances in Understanding Visual Processes ( Valberg A , Lee B , eds), pp 83\u201393. London: Plenum Press.","DOI":"10.1007\/978-1-4615-3718-2_10"},{"key":"2023092005300569000_2023.09.15.557995v1.73","doi-asserted-by":"crossref","first-page":"2633","DOI":"10.1364\/JOSAA.14.002633","article-title":"Postreceptoral chromatic detection mechanisms revealed by noise masking in three-dimensional cone contrast space","volume":"14","year":"1997","journal-title":"J Opt Soc Am A"},{"key":"2023092005300569000_2023.09.15.557995v1.74","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1364\/JOSAA.31.00A195","article-title":"Neurobiological hypothesis of color appearance and hue perception","volume":"31","year":"2014","journal-title":"J Opt Soc Am A"},{"key":"2023092005300569000_2023.09.15.557995v1.75","doi-asserted-by":"publisher","DOI":"10.1167\/16.2.7"},{"key":"2023092005300569000_2023.09.15.557995v1.76","first-page":"698","article-title":"Individual variability of neural computations in the primate retina","volume":"110","year":"2021","journal-title":"Neuron"},{"key":"2023092005300569000_2023.09.15.557995v1.77","doi-asserted-by":"publisher","DOI":"10.1167\/17.1.13"},{"key":"2023092005300569000_2023.09.15.557995v1.78","doi-asserted-by":"crossref","first-page":"1099","DOI":"10.1364\/JOSAA.34.001099","article-title":"Color opponency: tutorial","volume":"34","year":"2017","journal-title":"J Opt Soc Am A"},{"key":"2023092005300569000_2023.09.15.557995v1.79","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2017.01.005"},{"key":"2023092005300569000_2023.09.15.557995v1.80","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(04)00178-3"},{"key":"2023092005300569000_2023.09.15.557995v1.81","doi-asserted-by":"crossref","unstructured":"Soto F , Hsiang JC , Rajagopal R , Piggott K , Harocopos GJ , Couch SM , Custer P , Morgan JL , Kerschensteiner D (2020) Efficient coding by midget and parasol ganglion cells in the human retina. Neuron:1\u201311.","DOI":"10.1016\/j.neuron.2020.05.030"},{"key":"2023092005300569000_2023.09.15.557995v1.82","first-page":"1","article-title":"Color vision mechanisms","volume":"11","year":"2010","journal-title":"Opt Soc Am Handb Opt"},{"key":"2023092005300569000_2023.09.15.557995v1.83","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.2048-12.2012"},{"key":"2023092005300569000_2023.09.15.557995v1.84","doi-asserted-by":"publisher","DOI":"10.1016\/S0042-6989(97)00231-9"},{"key":"2023092005300569000_2023.09.15.557995v1.85","doi-asserted-by":"publisher","DOI":"10.1152\/jn.00714.2005"},{"key":"2023092005300569000_2023.09.15.557995v1.86","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.4682-07.2008"},{"key":"2023092005300569000_2023.09.15.557995v1.87","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.5338-07.2008"},{"key":"2023092005300569000_2023.09.15.557995v1.88","doi-asserted-by":"crossref","first-page":"1535","DOI":"10.1364\/JOSAA.17.001535","article-title":"Variations in normal color vision. I. Cone-opponent axes","volume":"17","year":"2000","journal-title":"J Opt Soc Am A"},{"key":"2023092005300569000_2023.09.15.557995v1.89","doi-asserted-by":"crossref","first-page":"1535","DOI":"10.1364\/JOSAA.17.001535","article-title":"Variations in normal color vision. II. Unique hues","volume":"17","year":"2000","journal-title":"J Opt Soc Am A"},{"key":"2023092005300569000_2023.09.15.557995v1.90","doi-asserted-by":"publisher","DOI":"10.1038\/353737a0"},{"key":"2023092005300569000_2023.09.15.557995v1.91","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(94)90028-0"},{"key":"2023092005300569000_2023.09.15.557995v1.92","doi-asserted-by":"crossref","first-page":"422","DOI":"10.1364\/JOSA.69.000422","article-title":"Opponent chromatic mechanisms: Relation to photopigments and hue naming","volume":"69","year":"1979","journal-title":"J Opt Soc Am"},{"key":"2023092005300569000_2023.09.15.557995v1.93","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(66)90078-2"},{"key":"2023092005300569000_2023.09.15.557995v1.94","doi-asserted-by":"crossref","first-page":"1307","DOI":"10.1364\/BOE.485371","article-title":"Evolution of adaptive optics retinal imaging [Invited]","volume":"14","year":"2023","journal-title":"Biomed Opt Express"},{"key":"2023092005300569000_2023.09.15.557995v1.95","doi-asserted-by":"publisher","DOI":"10.1364\/BOE.5.003174"},{"key":"2023092005300569000_2023.09.15.557995v1.96","doi-asserted-by":"publisher","DOI":"10.1167\/iovs.10-6250"},{"key":"2023092005300569000_2023.09.15.557995v1.97","doi-asserted-by":"publisher","DOI":"10.1523\/JNEUROSCI.4438-13.2014"},{"key":"2023092005300569000_2023.09.15.557995v1.98","doi-asserted-by":"publisher","DOI":"10.1016\/0042-6989(93)90239-S"},{"key":"2023092005300569000_2023.09.15.557995v1.99","doi-asserted-by":"publisher","DOI":"10.1007\/BF01185413"}],"container-title":[],"original-title":[],"link":[{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1101\/2023.09.15.557995","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,15]],"date-time":"2026-01-15T05:14:15Z","timestamp":1768454055000},"score":1,"resource":{"primary":{"URL":"http:\/\/biorxiv.org\/lookup\/doi\/10.1101\/2023.09.15.557995"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,9,16]]},"references-count":99,"URL":"https:\/\/doi.org\/10.1101\/2023.09.15.557995","relation":{"is-preprint-of":[{"id-type":"doi","id":"10.1523\/JNEUROSCI.1738-23.2024","asserted-by":"subject"}]},"subject":[],"published":{"date-parts":[[2023,9,16]]},"subtype":"preprint"}}