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Noise correlations improve response fidelity and stimulus encoding

Abstract

Computation in the nervous system often relies on the integration of signals from parallel circuits with different functional properties. Correlated noise in these inputs can, in principle, have diverse and dramatic effects on the reliability of the resulting computations1,2,3,4,5,6,7,8. Such theoretical predictions have rarely been tested experimentally because of a scarcity of preparations that permit measurement of both the covariation of a neuron’s input signals and the effect on a cell’s output of manipulating such covariation. Here we introduce a method to measure covariation of the excitatory and inhibitory inputs a cell receives. This method revealed strong correlated noise in the inputs to two types of retinal ganglion cell. Eliminating correlated noise without changing other input properties substantially decreased the accuracy with which a cell’s spike outputs encoded light inputs. Thus, covariation of excitatory and inhibitory inputs can be a critical determinant of the reliability of neural coding and computation.

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Figure 1: Effects of noise correlations on the variability of synaptic current and spike output.
Figure 2: Near-simultaneous recording of excitatory and inhibitory synaptic input to an ON–OFF directionally selective ganglion cell.
Figure 3: Strength and impact of noise correlations in synaptic inputs to primate midget ganglion cells.
Figure 4: Strength and impact of noise correlations in synaptic inputs to ON–OFF directionally selective ganglion cells.

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Acknowledgements

We thank D. Dacey, O. Packer, J. Crook, B. Peterson and T. Haun for providing primate tissue; P. Newman and E. Martinson for technical assistance; T. Azevedo, E. J. Chichilnisky, F. Dunn, G. Murphy, S. Kuo, E. Shea-Brown, M. Shadlen and W. Spain for comments on the manuscript and discussions. Support was provided by HHMI and NIH (EY-11850).

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J.C. and F.R. designed and carried out the experiments, J.C. analysed the data and J.C. and F.R. wrote the paper.

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Correspondence to Fred Rieke.

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The authors declare no competing financial interests.

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Cafaro, J., Rieke, F. Noise correlations improve response fidelity and stimulus encoding. Nature 468, 964–967 (2010). https://doi.org/10.1038/nature09570

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