Abstract
Transduction and synaptic noise generated in retinal cone photoreceptors determine the fidelity with which light inputs are encoded, and the readout of cone signals by downstream circuits determines whether this fidelity is used for vision. We examined the effect of cone noise on visual signals by measuring its contribution to correlated noise in primate retinal ganglion cells. Correlated noise was strong in the responses of dissimilar cell types with shared cone inputs. The dynamics of cone noise could account for rapid correlations in ganglion cell activity, and the extent of shared cone input could explain correlation strength. Furthermore, correlated noise limited the fidelity with which visual signals were encoded by populations of ganglion cells. Thus, a simple picture emerges: cone noise, traversing the retina through diverse pathways, accounts for most of the noise and correlations in the retinal output and constrains how higher centers exploit signals carried by parallel visual pathways.
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References
Mollon, J.D., Astell, S. & Cavonius, C.R. A reduction in stimulus duration can improve wavelength discriminations mediated by short-wave cones. Vision Res. 32, 745–755 (1992).
Westheimer, G. Visual hyperacuity. Prog. Sens. Physiol. 1, 1–30 (1981).
Barlow, H.B. Purkinje shift and retinal noise. Nature 179, 255–256 (1957).
Donner, K. Noise and the absolute thresholds of cone and rod vision. Vision Res. 32, 853–866 (1992).
Barlow, H.B. Retinal noise and absolute threshold. J. Opt. Soc. Am. 46, 634–639 (1956).
Aho, A.C., Donner, K., Hyden, C., Reuter, T. & Orlov, O.Y. Retinal noise, the performance of retinal ganglion cells, and visual sensitivity in the dark-adapted frog. J. Opt. Soc. Am. A 4, 2321–2329 (1987).
Naarendorp, F. et al. Dark light, rod saturation, and the absolute and incremental sensitivity of mouse cone vision. J. Neurosci. 30, 12495–12507 (2010).
Schneeweis, D.M. & Schnapf, J.L. The photovoltage of macaque cone photoreceptors: adaptation, noise and kinetics. J. Neurosci. 19, 1203–1216 (1999).
Fu, Y., Kefalov, V., Luo, D.G., Xue, T. & Yau, K.W. Quantal noise from human red cone pigment. Nat. Neurosci. 11, 565–571 (2008).
Choi, S.Y. et al. Encoding light intensity by the cone photoreceptor synapse. Neuron 48, 555–562 (2005).
Borghuis, B.G., Sterling, P. & Smith, R.G. Loss of sensitivity in an analog neural circuit. J. Neurosci. 29, 3045–3058 (2009).
Mastronarde, D.N. Correlated firing of retinal ganglion cells. Trends Neurosci. 12, 75–80 (1989).
Meister, M. Multineuronal codes in retinal signaling. Proc. Natl. Acad. Sci. USA 93, 609–614 (1996).
Field, G.D. & Chichilnisky, E.J. Information processing in the primate retina: circuitry and coding. Annu. Rev. Neurosci. 30, 1–30 (2007).
Puchalla, J.L., Schneidman, E., Harris, R.A. & Berry, M.J. Redundancy in the population code of the retina. Neuron 46, 493–504 (2005).
Mastronarde, D.N. Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. J. Neurophysiol. 49, 325–349 (1983).
Mastronarde, D.N. Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. J. Neurophysiol. 49, 303–324 (1983).
DeVries, S.H. Correlated firing in rabbit retinal ganglion cells. J. Neurophysiol. 81, 908–920 (1999).
Brivanlou, I.H., Warland, D.K. & Meister, M. Mechanisms of concerted firing among retinal ganglion cells. Neuron 20, 527–539 (1998).
Lamb, T.D. & Simon, E.J. Analysis of electrical noise in turtle cones. J. Physiol. (Lond.) 272, 435–468 (1977).
Jackman, S.L. et al. Role of the synaptic ribbon in transmitting the cone light response. Nat. Neurosci. 12, 303–310 (2009).
Dunn, F.A., Lankheet, M.J. & Rieke, F. Light adaptation in cone vision involves switching between receptor and post-receptor sites. Nature 449, 603–606 (2007).
Goodchild, A.K., Ghosh, K.K. & Martin, P.R. Comparison of photoreceptor spatial density and ganglion cell morphology in the retina of human, macaque monkey, cat and the marmoset Callithrix jacchus. J. Comp. Neurol. 366, 55–75 (1996).
Werblin, F.S. & Dowling, J.E. Organization of the retina of the mudpuppy, Necturus maculosus. II. Intracellular recording. J. Neurophysiol. 32, 339–355 (1969).
Boycott, B.B. & Wassle, H. Morphological classification of bipolar cells of the primate retina. Eur. J. Neurosci. 3, 1069–1088 (1991).
Trong, P.K. & Rieke, F. Origin of correlated activity between parasol retinal ganglion cells. Nat. Neurosci. 11, 1343–1351 (2008).
Zaghloul, K.A., Boahen, K. & Demb, J.B. Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. J. Neurosci. 23, 2645–2654 (2003).
Slaughter, M.M. & Miller, R.F. 2-amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science 211, 182–185 (1981).
Rentería, R.C. et al. Intrinsic ON responses of the retinal OFF pathway are suppressed by the ON pathway. J. Neurosci. 26, 11857–11869 (2006).
Dacey, D.M. & Brace, S. A coupled network for parasol but not midget ganglion cells in the primate retina. Vis. Neurosci. 9, 279–290 (1992).
Shlens, J., Rieke, F. & Chichilnisky, E. Synchronized firing in the retina. Curr. Opin. Neurobiol. 18, 396–402 (2008).
Baylor, D.A. & Fettiplace, R. Kinetics of synaptic transfer from receptors to ganglion cells in turtle retina. J. Physiol. (Lond.) 271, 425–448 (1977).
Gauthier, J.L. et al. Uniform signal redundancy of parasol and midget ganglion cells in primate retina. J. Neurosci. 29, 4675–4680 (2009).
Cohen, E. & Sterling, P. Parallel circuits from cones to the on-beta ganglion cell. Eur. J. Neurosci. 4, 506–520 (1992).
Xu, Y., Vasudeva, V., Vardi, N., Sterling, P. & Freed, M.A. Different types of ganglion cell share a synaptic pattern. J. Comp. Neurol. 507, 1871–1878 (2008).
Shadlen, M.N., Britten, K.H., Newsome, W.T. & Movshon, J.A. A computational analysis of the relationship between neuronal and behavioral responses to visual motion. J. Neurosci. 16, 1486–1510 (1996).
Field, G.D., Sampath, A.P. & Rieke, F. Retinal processing near absolute threshold: from behavior to mechanism. Annu. Rev. Physiol. 67, 491–514 (2005).
Hamer, R.D., Nicholas, S.C., Tranchina, D., Liebman, P.A. & Lamb, T.D. Multiple steps of phosphorylation of activated rhodopsin can account for the reproducibility of vertebrate rod single-photon responses. J. Gen. Physiol. 122, 419–444 (2003).
Vaney, D.I. Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin. Neurosci. Lett. 125, 187–190 (1991).
Hu, E.H. & Bloomfield, S.A. Gap junctional coupling underlies the short-latency spike synchrony of retinal alpha ganglion cells. J. Neurosci. 23, 6768–6777 (2003).
Hidaka, S., Akahori, Y. & Kurosawa, Y. Dendrodendritic electrical synapses between mammalian retinal ganglion cells. J. Neurosci. 24, 10553–10567 (2004).
Dacey, D.M. & Packer, O.S. Color coding in the primate retina: diverse cell types and cone-specific circuitry. Curr. Opin. Neurobiol. 13, 421–427 (2003).
Field, G.D. et al. Spatial properties and functional organization of small bistratified ganglion cells in primate retina. J. Neurosci. 27, 13261–13272 (2007).
Pillow, J.W. et al. Spatio-temporal correlations and visual signaling in a complete neuronal population. Nature 454, 995–999 (2008).
Gollisch, T. & Meister, M. Rapid neural coding in the retina with relative spike latencies. Science 319, 1108–1111 (2008).
Rieke, F. Spikes: Exploring the Neural Code (MIT Press, Cambridge, Massachusetts, 1997).
Bialek, W., Rieke, F., de Ruyter van Steveninck, R.R. & Warland, D. Reading a neural code. Science 252, 1854–1857 (1991).
Warland, D.K., Reinagel, P. & Meister, M. Decoding visual information from a population of retinal ganglion cells. J. Neurophysiol. 78, 2336–2350 (1997).
Chichilnisky, E.J. A simple white noise analysis of neuronal light responses. Network 12, 199–213 (2001).
Acknowledgements
We thank G. Horwitz, G. Murphy, L. Paninski and M. Vidne for detailed comments on the manuscript and helpful discussions, D. Carleton, E. Martinson and P. Newman for excellent technical assistance, G.D. Field, J.L. Gauthier, J. Shlens and A. Sher for experimental assistance, A.M. Litke, M.I. Grivich, D.Petrusca, W. Dabrowski, A. Grillo, P. Grybos, P. Hottowy and S. Kachiguine for technical development, and J. Crook, D. Dacey, T. Haun, M. Manookin, O. Packer, B. Peterson, H. Fox, K. Osborn and the Tissue Distribution Program of the Regional Primate Research Center at the University of Washington for providing primate tissue. This work was supported by the Howard Hughes Medical Institute (F.R.), the US National Institutes of Health (EY-11850 to F.R. and EY-13150 to E.J.C.), the Academy of Finland (grant 123231 to P.A.-L.), the McKnight Foundation (E.J.C.) and a Pioneer Postdoctoral Fellowship Award (M.G.).
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P.A.-L., M.G., E.J.C. and F.R. designed and performed experiments. M.G. and F.R. analyzed data. P.A.-L., M.G., E.J.C. and F.R. wrote the manuscript.
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Ala-Laurila, P., Greschner, M., Chichilnisky, E. et al. Cone photoreceptor contributions to noise and correlations in the retinal output. Nat Neurosci 14, 1309–1316 (2011). https://doi.org/10.1038/nn.2927
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DOI: https://doi.org/10.1038/nn.2927
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