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Functional connectivity in the retina at the resolution of photoreceptors

Author

Listed:
  • Greg D. Field

    (Systems Neurobiology Laboratories, Salk Institute for Biological Studies)

  • Jeffrey L. Gauthier

    (Systems Neurobiology Laboratories, Salk Institute for Biological Studies
    Present addresses: Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey 08544, USA (J.L.G.); Department of Statistics and Center for Theoretical Neuroscience, Columbia University, New York, New York 10027, USA (T.A.M.).)

  • Alexander Sher

    (Santa Cruz Institute for Particle Physics, University of California)

  • Martin Greschner

    (Systems Neurobiology Laboratories, Salk Institute for Biological Studies)

  • Timothy A. Machado

    (Systems Neurobiology Laboratories, Salk Institute for Biological Studies
    Present addresses: Princeton Neuroscience Institute, Princeton University, Princeton, New Jersey 08544, USA (J.L.G.); Department of Statistics and Center for Theoretical Neuroscience, Columbia University, New York, New York 10027, USA (T.A.M.).)

  • Lauren H. Jepson

    (Systems Neurobiology Laboratories, Salk Institute for Biological Studies)

  • Jonathon Shlens

    (Systems Neurobiology Laboratories, Salk Institute for Biological Studies)

  • Deborah E. Gunning

    (University of Glasgow)

  • Keith Mathieson

    (University of Glasgow)

  • Wladyslaw Dabrowski

    (Faculty of Physics and Applied Computer Science, AGH University of Science and Technology)

  • Liam Paninski

    (Columbia University)

  • Alan M. Litke

    (Santa Cruz Institute for Particle Physics, University of California)

  • E. J. Chichilnisky

    (Systems Neurobiology Laboratories, Salk Institute for Biological Studies)

Abstract

To understand a neural circuit requires knowledge of its connectivity. Here we report measurements of functional connectivity between the input and ouput layers of the macaque retina at single-cell resolution and the implications of these for colour vision. Multi-electrode technology was used to record simultaneously from complete populations of the retinal ganglion cell types (midget, parasol and small bistratified) that transmit high-resolution visual signals to the brain. Fine-grained visual stimulation was used to identify the location, type and strength of the functional input of each cone photoreceptor to each ganglion cell. The populations of ON and OFF midget and parasol cells each sampled the complete population of long- and middle-wavelength-sensitive cones. However, only OFF midget cells frequently received strong input from short-wavelength-sensitive cones. ON and OFF midget cells showed a small non-random tendency to selectively sample from either long- or middle-wavelength-sensitive cones to a degree not explained by clumping in the cone mosaic. These measurements reveal computations in a neural circuit at the elementary resolution of individual neurons.

Suggested Citation

  • Greg D. Field & Jeffrey L. Gauthier & Alexander Sher & Martin Greschner & Timothy A. Machado & Lauren H. Jepson & Jonathon Shlens & Deborah E. Gunning & Keith Mathieson & Wladyslaw Dabrowski & Liam Pa, 2010. "Functional connectivity in the retina at the resolution of photoreceptors," Nature, Nature, vol. 467(7316), pages 673-677, October.
    • Handle: RePEc:nat:nature:v:467:y:2010:i:7316:d:10.1038_nature09424
    DOI: 10.1038/nature09424
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    Cited by:

    1. Marvin Seifert & Paul A. Roberts & George Kafetzis & Daniel Osorio & Tom Baden, 2023. "Birds multiplex spectral and temporal visual information via retinal On- and Off-channels," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Noah C Benson & Jeremy R Manning & David H Brainard, 2014. "Unsupervised Learning of Cone Spectral Classes from Natural Images," PLOS Computational Biology, Public Library of Science, vol. 10(6), pages 1-13, June.
    3. Eric G. Wu & Nora Brackbill & Colleen Rhoades & Alexandra Kling & Alex R. Gogliettino & Nishal P. Shah & Alexander Sher & Alan M. Litke & Eero P. Simoncelli & E. J. Chichilnisky, 2024. "Fixational eye movements enhance the precision of visual information transmitted by the primate retina," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Riccardo Manzotti, 2017. "A Perception-Based Model of Complementary Afterimages," SAGE Open, , vol. 7(1), pages 21582440166, January.
    5. James Trousdale & Yu Hu & Eric Shea-Brown & Krešimir Josić, 2012. "Impact of Network Structure and Cellular Response on Spike Time Correlations," PLOS Computational Biology, Public Library of Science, vol. 8(3), pages 1-15, March.
    6. Miranda L. Scalabrino & Mishek Thapa & Tian Wang & Alapakkam P. Sampath & Jeannie Chen & Greg D. Field, 2023. "Late gene therapy limits the restoration of retinal function in a mouse model of retinitis pigmentosa," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    7. Peichao Li & Anupam K. Garg & Li A. Zhang & Mohammad S. Rashid & Edward M. Callaway, 2022. "Cone opponent functional domains in primary visual cortex combine signals for color appearance mechanisms," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

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