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Cone photoreceptor contributions to noise and correlations in the retinal output

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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Figure 1: Covariation of excitatory inputs to cells that share little known circuitry.
Figure 2: Effect of APB and mixture of LY341495 and APB on light responses of ON parasol ganglion cells.
Figure 3: Correlated and total noise in ganglion cell excitatory synaptic inputs are dominated by cone noise.
Figure 4: Rapid fluctuations in cone voltage are conveyed to ganglion cells.
Figure 5: Dendritic overlap predicts correlation strength.
Figure 6: Shared noise limits fidelity of neural coding in populations of ganglion cells.
Figure 7: Dependence of predicted correlation strength on model parameters.

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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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Correspondence to Fred Rieke.

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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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