Letter

Topology of ON and OFF inputs in visual cortex enables an invariant columnar architecture

  • Nature volume 533, pages 9094 (05 May 2016)
  • doi:10.1038/nature17941
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Abstract

Circuits in the visual cortex integrate the information derived from separate ON (light-responsive) and OFF (dark-responsive) pathways to construct orderly columnar representations of stimulus orientation and visual space1,2,3,4,5,6,7. How this transformation is achieved to meet the specific topographic constraints of each representation remains unclear. Here we report several novel features of ON–OFF convergence visualized by mapping the receptive fields of layer 2/3 neurons in the tree shrew (Tupaia belangeri) visual cortex using two-photon imaging of GCaMP6 calcium signals. We show that the spatially separate ON and OFF subfields of simple cells in layer 2/3 exhibit topologically distinct relationships with the maps of visual space and orientation preference. The centres of OFF subfields for neurons in a given region of cortex are confined to a compact region of visual space and display a smooth visuotopic progression. By contrast, the centres of the ON subfields are distributed over a wider region of visual space, display substantial visuotopic scatter, and have an orientation-specific displacement consistent with orientation preference map structure. As a result, cortical columns exhibit an invariant aggregate receptive field structure: an OFF-dominated central region flanked by ON-dominated subfields. This distinct arrangement of ON and OFF inputs enables continuity in the mapping of both orientation and visual space and the generation of a columnar map of absolute spatial phase.

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Acknowledgements

We thank members of the Fitzpatrick laboratory for discussions and comments, D. Ouimet and K. Diah for animal technical support, T. Walker for technical assistance, A. Jacob for histology assistance, D. Wilson for advice on two-photon imaging, and D. Whitney for advice on epi-fluorescence imaging. This work was supported by grants from the US National Institutes of Health and funding from Max Planck Florida Institute for Neuroscience and Max Planck Society to D.F.

Author information

Affiliations

  1. Department of Functional Architecture and Development of Cerebral Cortex, Max Planck Florida Institute for Neuroscience, Jupiter, Florida 33458, USA

    • Kuo-Sheng Lee
    • , Xiaoying Huang
    •  & David Fitzpatrick
  2. Integrative Biology and Neuroscience Graduate Program, Florida Atlantic University, Boca Raton, Florida 33431, USA

    • Kuo-Sheng Lee

Authors

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Contributions

K.-S.L. and D.F. designed the experiments. X.H. helped to collect data in the initial stage. K.-S.L performed all the experiments and analysed all the data with assistance from X.H. K.-S.L. and D.F. wrote the manuscript with input from X.H.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to David Fitzpatrick.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Data

    This file contains the statistical details of experimental analysis.

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