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Coding of stimulus sequences by population responses in visual cortex

Nature Neuroscience volume 12, pages 1317–1324 (2009)Cite this article

Abstract

Neuronal populations in sensory cortex represent time-changing sensory input through a spatiotemporal code. What are the rules that govern this code? We measured membrane potentials and spikes from neuronal populations in cat visual cortex (V1) using voltage-sensitive dyes and electrode arrays. We first characterized the population response to a single orientation. As response amplitude grew, the population tuning width remained constant for membrane potential responses and became progressively sharper for spike responses. We then asked how these single-orientation responses combine to code for successive orientations. We found that they combined through simple linear summation. Linearity, however, was violated after stimulus offset, when responses exhibited an unexplained persistence. As a result of linearity, the interactions between responses to successive stimuli were minimal. Our results indicate that higher cortical areas may reconstruct the stimulus sequence from V1 population responses through a simple instantaneous decoder. Therefore, spatial and temporal codes in area V1 operate largely independently.

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Figure 1: Population responses to an oriented stimulus.
Figure 2: Properties of single-orientation responses.
Figure 3: Predicting the membrane potential responses of the population to the full stimulus sequence.
Figure 4: Predicting the spike responses of the population to the full stimulus sequence.
Figure 5: Predicting the interactions between population responses to successive orientations.
Figure 6: Unexplained persistence of population responses after stimulus offset.
Figure 7: Decoding stimulus orientation from the population responses.

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Acknowledgements

We thank I. Nauhaus, R.A. Frazor, L. Busse and S. Katzner for help with data acquisition. We thank W.T. Newsome, W.S. Geisler and G. Felsen for helpful discussions. This work was supported by a Scholar Award from the McKnight Endowment Fund for Neuroscience (M.C.) and by US National Institutes of Health grants EY017396 (M.C.) and EY018322 (D.L.R.). M.C. holds the GlaxoSmithKline/Fight for Sight Chair in Visual Neuroscience.

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Authors and Affiliations

  1. University College London Institute of Ophthalmology, University College London, London, UK

    Andrea Benucci & Matteo Carandini

  2. Smith-Kettlewell Eye Research Institute, San Francisco, California, USA

    Andrea Benucci & Matteo Carandini

  3. Departments of Neurobiology and Psychology, Jules Stein Eye Institute, University of California Los Angeles, Los Angeles, California, USA

    Dario L Ringach

Authors
  1. Andrea Benucci
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  2. Dario L Ringach
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Contributions

A.B. and M.C. carried out the experiments, A.B. analyzed the data, and all of the authors contributed to the intellectual development of the project and to the writing of the manuscript.

Corresponding author

Correspondence to Andrea Benucci.

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Supplementary Figures 1–3 (PDF 260 kb)

Supplementary Video 1

Decoding the population responses to recover the stimulus orientation. (AVI 6151 kb)

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Benucci, A., Ringach, D. & Carandini, M. Coding of stimulus sequences by population responses in visual cortex. Nat Neurosci 12, 1317–1324 (2009). https://doi.org/10.1038/nn.2398

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