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Spatio-temporal correlations and visual signalling in a complete neuronal population

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Abstract

Statistical dependencies in the responses of sensory neurons govern both the amount of stimulus information conveyed and the means by which downstream neurons can extract it. Although a variety of measurements indicate the existence of such dependencies1,2,3, their origin and importance for neural coding are poorly understood. Here we analyse the functional significance of correlated firing in a complete population of macaque parasol retinal ganglion cells using a model of multi-neuron spike responses4,5. The model, with parameters fit directly to physiological data, simultaneously captures both the stimulus dependence and detailed spatio-temporal correlations in population responses, and provides two insights into the structure of the neural code. First, neural encoding at the population level is less noisy than one would expect from the variability of individual neurons: spike times are more precise, and can be predicted more accurately when the spiking of neighbouring neurons is taken into account. Second, correlations provide additional sensory information: optimal, model-based decoding that exploits the response correlation structure extracts 20% more information about the visual scene than decoding under the assumption of independence, and preserves 40% more visual information than optimal linear decoding6. This model-based approach reveals the role of correlated activity in the retinal coding of visual stimuli, and provides a general framework for understanding the importance of correlated activity in populations of neurons.

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Figure 1: Multi-neuron encoding model and fitted parameters.
Figure 2: Analysis of response correlations.
Figure 3: Spike-train prediction comparison.
Figure 4: Decoding performance comparison.

Change history

  • 19 September 2008

    In the online-only extended Methods, two equations were corrected on 19 September 2008. Please see the erratum at the end of the PDF for details.

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Acknowledgements

We thank M. Bethge, C. Brody, D. Butts, P. Latham, M. Lengyel, S. Nirenberg and R. Sussman for comments and discussions; G. Field, M. Greschner, J. Gauthier and C. Hulse for experimental assistance; M. I. Grivich, D. Petrusca, W. Dabrowski, A. Grillo, P. Grybos, P. Hottowy and S. Kachiguine for technical development; H. Fox, M. Taffe, E. Callaway and K. Osborn for providing access to retinas; and S. Barry for machining. Funding was provided a Royal Society USA/Canada Research Fellowship (J.W.P.); NSF IGERT DGE-03345 (J.S.); NEI grant EY018003 (E.J.C., L.P. and E.P.S.); Gatsby Foundation Pilot Grant (L.P.); Burroughs Wellcome Fund Career Award at the Scientific Interface (A.S.); US National Science Foundation grant PHY-0417175 (A.M.L.); McKnight Foundation (A.M.L. and E.J.C.); and HHMI (J.W.P., L.P. and E.P.S.).

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Correspondence to Jonathan W. Pillow.

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Pillow, J., Shlens, J., Paninski, L. et al. Spatio-temporal correlations and visual signalling in a complete neuronal population. Nature 454, 995–999 (2008). https://doi.org/10.1038/nature07140

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