Abstract
Human vision starts with the activation of rod photoreceptors in dim light and short (S)-, medium (M)-, and long (L)- wavelength-sensitive cone photoreceptors in daylight. Recently a parallel, non-rod, non-cone photoreceptive pathway, arising from a population of retinal ganglion cells, was discovered in nocturnal rodents1. These ganglion cells express the putative photopigment melanopsin and by signalling gross changes in light intensity serve the subconscious, ‘non-image-forming’ functions of circadian photoentrainment and pupil constriction1,2,3,4,5,6,7. Here we show an anatomically distinct population of ‘giant’, melanopsin-expressing ganglion cells in the primate retina that, in addition to being intrinsically photosensitive, are strongly activated by rods and cones, and display a rare, S-Off, (L + M)-On type of colour-opponent receptive field. The intrinsic, rod and (L + M) cone-derived light responses combine in these giant cells to signal irradiance over the full dynamic range of human vision. In accordance with cone-based colour opponency, the giant cells project to the lateral geniculate nucleus, the thalamic relay to primary visual cortex. Thus, in the diurnal trichromatic primate, ‘non-image-forming’ and conventional ‘image-forming’ retinal pathways are merged, and the melanopsin-based signal might contribute to conscious visual perception.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Berson, D. M., Dunn, F. A. & Takao, M. Phototransduction by retinal ganglion cells that set the circadian clock. Science 295, 1070–1073 (2002)
Hattar, S. et al. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature 424, 75–81 (2003)
Lucas, R. J. et al. Diminished pupillary light reflex at high irradiances in melanopsin-knockout mice. Science 299, 245–247 (2003)
Panda, S. et al. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298, 2213–2216 (2002)
Ruby, N. F. et al. Role of melanopsin in circadian responses to light. Science 298, 2211–2213 (2002)
Hattar, S., Liao, H. W., Takao, M., Berson, D. M. & Yau, K. W. Melanopsin-containing retinal ganglion cells: architecture, projections, and intrinsic photosensitivity. Science 295, 1065–1070 (2002)
Panda, S. et al. Melanopsin is required for non-image-forming photic responses in blind mice. Science 301, 525–527 (2003)
Thapan, K., Arendt, J. & Skene, D. J. An action spectrum for melatonin suppression: evidence for a novel non-rod, non-cone photoreceptor system in humans. J. Physiol. (Lond.) 535, 261–267 (2001)
Provencio, I. et al. A novel human opsin in the inner retina. J. Neurosci. 20, 600–605 (2000)
Brainard, G. C. et al. Action spectrum for melatonin regulation in humans: evidence for a novel circadian photoreceptor. J. Neurosci. 21, 6405–6412 (2001)
Hankins, M. W. & Lucas, R. J. The primary visual pathway in humans is regulated according to long-term light exposure through the action of a nonclassical photopigment. Curr. Biol. 12, 191–198 (2002)
Hannibal, J. et al. Melanopsin is expressed in PACAP-containing retinal ganglion cells of the human retinohypothalamic tract. Invest. Ophthalmol. Vis. Sci. 45, 4202–4209 (2004)
Dacey, D., Peterson, B., Robinson, F. & Gamlin, P. Fireworks in the primate retina: in vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15–27 (2003)
Dacey, D. M. & Lee, B. B. The blue-ON opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735 (1994)
Hood, D. C. & Finkelstein, M. A. in Handbook of Perception and Human Performance Vol. 1 (eds Boff, K. R., Kaufman, L. & Thomas, J. P.) Ch. 5, 1–66 (John Wiley and Sons, New York, 1986)
Takahashi, J. S., DeCoursey, P. J., Bauman, L. & Menaker, M. Spectral sensitivity of a novel photoreceptive system mediating entrainment of mammalian circadian rhythms. Nature 308, 186–188 (1984)
Fain, G. L., Matthews, H. R., Cornwall, M. C. & Koutalos, Y. Adaptation in vertebrate photoreceptors. Physiol. Rev. 81, 117–151 (2001)
Mollon, J. D. & Jordan, G. Eine evolutionare Interpretation des menschlichen Farbensehens. Die Farbe 35/36, 139–170 (1989)
Valberg, A., Lee, B. B. & Tigwell, D. A. Neurones with strong inhibitory s-cone inputs in the macaque lateral geniculate nucleus. Vision Res. 26, 1061–1064 (1986)
Cottaris, N. & DeValois, R. Temporal dynamics of chromatic tuning in macaque primary visual cortex. Nature 395, 896–900 (1998)
Krauskopf, J., Williams, D. R. & Heeley, D. W. Cardinal directions of color space. Vision Res. 22, 1123–1131 (1982)
Klug, K., Herr, S., Ngo, I. T., Sterling, P. & Schein, S. Macaque retina contains an S-cone OFF midget pathway. J. Neurosci. 23, 9881–9887 (2003)
Barlow, H. B. & Levick, W. R. Changes in the maintained discharge with adaptation level in the cat retina. J. Physiol. (Lond.) 202, 699–718 (1969)
Marrocco, R. T. Possible neural basis of brightness magnitude estimations. Brain Res. 86, 128–133 (1975)
Kayama, Y., Riso, R. R., Bartlett, J. R. & Doty, R. W. Luxotonic responses of units in macaque striate cortex. J. Neurophysiol. 42, 1495–1517 (1979)
Kinoshita, M. & Komatsu, H. Neural representation of the luminance and brightness of a uniform surface in the macaque primary visual cortex. J. Neurophysiol. 86, 2559–2570 (2001)
Barlow, R. B. Jr & Verrillo, R. T. Brightness sensation in a ganzfeld. Vision Res. 16, 1291–1297 (1976)
Packer, O. et al. Characterization and use of a digital light projector for vision research. Vision Res. 41, 427–439 (2001)
Diller, L. et al. L and M cone contributions to the midget and parasol ganglion cell receptive fields of macaque monkey retina. J. Neurosci. 24, 1079–1088 (2004)
Enroth-Cugell, C., Robson, J. G., Schweitzer-Tong, D. E. & Watson, A. B. Spatio-temporal interactions in cat retinal ganglion cells showing linear spatial summation. J. Physiol. (Lond.) 341, 279–307 (1983)
Acknowledgements
We woud like to thank C. Curcio and the Age-Related Maculopathy Histopathology Laboratory (supported by the International Retinal Research Foundation, the National Eye Institute and the Vision Science Research Center), University of Alabama at Birmingham for the human retinae used in the immunohistochemical studies. Macaque retinae were provided by the Tissue Distribution program of the National Primate Research Center at the University of Washington. We thank O. Packer and T. Haun for technical assistance. Supported by US National Eye Institute grants to D.M.D., J.P., K.-W.Y., H.W.-L. and F.R.R., Vision Research Center Core grants to D.M.D. and P.D.G., an Alabama EyeSight Foundation award to P.D.G. and a Retina Research Foundation Paul Kayser Award to D.M.D.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Rights and permissions
About this article
Cite this article
Dacey, D., Liao, HW., Peterson, B. et al. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433, 749–754 (2005). https://doi.org/10.1038/nature03387
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature03387
This article is cited by
-
Targeting sleep and the circadian system as a novel treatment strategy for Parkinson’s disease
Journal of Neurology (2024)
-
A Comprehensive Overview of the Neural Mechanisms of Light Therapy
Neuroscience Bulletin (2024)
-
Melanopsin-mediated optical entrainment regulates circadian rhythms in vertebrates
Communications Biology (2023)
-
Neural correlates of visual and tactile path integration and their task related modulation
Scientific Reports (2023)
-
Blue-light background impairs visual exogenous attention shift
Scientific Reports (2023)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.