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Sublinear integration underlies binocular processing in primary visual cortex

Nature Neuroscience volume 16, pages 714–723 (2013)Cite this article

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Abstract

Although we know much about the capacity of neurons to integrate synaptic inputs in vitro, less is known about synaptic integration in vivo. Here we address this issue by investigating the integration of inputs from the two eyes in mouse primary visual cortex. We find that binocular inputs to layer 2/3 pyramidal neurons are integrated sublinearly in an amplitude-dependent manner. Sublinear integration was greatest when binocular responses were largest, as occurs at the preferred orientation and binocular disparity, and highest contrast. Using voltage-clamp experiments and modeling, we show that sublinear integration occurs postsynaptically. The extent of sublinear integration cannot be accounted for solely by nonlinear integration of excitatory inputs, even when they are activated closely in space and time, but requires balanced recruitment of inhibition. Finally, we show that sublinear binocular integration acts as a divisive form of gain control, linearizing the output of binocular neurons and enhancing orientation selectivity.

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Figure 1: Summation of binocular inputs at the preferred orientation.
Figure 2: Dependence of binocular integration on stimulus orientation and response phase.
Figure 3: Dependence of binocular integration on phase disparity.
Figure 4: Summation of different components of the synaptic response.
Figure 5: Recruitment and summation of excitation and inhibition during binocular integration.
Figure 6: Balanced recruitment of excitation and inhibition explains sublinear integration of binocular synaptic inputs.
Figure 7: Interactions between excitatory synapses alone cannot account for sublinear integration of binocular inputs.
Figure 8: Impact of sublinear binocular integration on action potential output.

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Acknowledgements

We are grateful to S. Solomon for discussions. We would also like to thank T. Bock for help with Matlab programming. This work was supported by the Swiss National Science Foundation, the Australian National Health and Medical Research Council and the John Curtin School of Medical Research.

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Authors and Affiliations

  1. Eccles Institute of Neuroscience, John Curtin School of Medical Research, Australian National University, Canberra, Australian Capital Territory, Australia

    Fabio Longordo, Minh-Son To, Kaori Ikeda & Greg J Stuart

  2. Department of Human Physiology and Centre for Neuroscience, Flinders University Adelaide, South Australia, Australia

    Minh-Son To

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  1. Fabio Longordo
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Contributions

G.J.S. and F.L. conceived the project. F.L. conducted the experiments and performed all analysis. K.I. contributed to early experiments. M.-S.T. performed all simulations. All authors discussed the data and contributed to writing the manuscript.

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Correspondence to Fabio Longordo or Greg J Stuart.

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Longordo, F., To, MS., Ikeda, K. et al. Sublinear integration underlies binocular processing in primary visual cortex. Nat Neurosci 16, 714–723 (2013). https://doi.org/10.1038/nn.3394

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