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Mechanisms and circuitry underlying directional selectivity in the retina

Author

Listed:
  • Shelley I. Fried

    (Vision Science, University of California Berkeley)

  • Thomas A. Münch

    (University of California Berkeley)

  • Frank S. Werblin

    (University of California Berkeley)

Abstract

In the retina, directionally selective ganglion cells respond with robust spiking to movement in their preferred direction, but show minimal response to movement in the opposite, or null, direction1,2. The mechanisms and circuitry underlying this computation have remained controversial3. Here we show, by isolating the excitatory and inhibitory inputs to directionally selective cells and measuring direct connections between these cells and presynaptic neurons, that a presynaptic interneuron, the starburst amacrine cell, delivers direct inhibition to directionally selective cells. The processes of starburst cells are connected asymmetrically to directionally selective cells: those pointing in the null direction deliver inhibition; those pointing in the preferred direction do not. Starburst cells project inhibition laterally ahead of a stimulus moving in the null direction. In addition, starburst inhibition is itself directionally selective: it is stronger for movement in the null direction. Excitation in response to null direction movement is reduced by an inhibitory signal acting at a site that is presynaptic to the directionally selective cell. The interplay of these components generates reduced excitation and enhanced inhibition in the null direction, thereby ensuring robust directional selectivity.

Suggested Citation

  • Shelley I. Fried & Thomas A. Münch & Frank S. Werblin, 2002. "Mechanisms and circuitry underlying directional selectivity in the retina," Nature, Nature, vol. 420(6914), pages 411-414, November.
  • Handle: RePEc:nat:nature:v:420:y:2002:i:6914:d:10.1038_nature01179
    DOI: 10.1038/nature01179
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    Cited by:

    1. John A. Gaynes & Samuel A. Budoff & Michael J. Grybko & Joshua B. Hunt & Alon Poleg-Polsky, 2022. "Classical center-surround receptive fields facilitate novel object detection in retinal bipolar cells," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Elishai Ezra-Tsur & Oren Amsalem & Lea Ankri & Pritish Patil & Idan Segev & Michal Rivlin-Etzion, 2021. "Realistic retinal modeling unravels the differential role of excitation and inhibition to starburst amacrine cells in direction selectivity," PLOS Computational Biology, Public Library of Science, vol. 17(12), pages 1-31, December.
    3. Jason S Prentice & Olivier Marre & Mark L Ioffe & Adrianna R Loback & Gašper Tkačik & Michael J Berry II, 2016. "Error-Robust Modes of the Retinal Population Code," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-32, November.
    4. Héctor Acarón Ledesma & Jennifer Ding & Swen Oosterboer & Xiaolin Huang & Qiang Chen & Sui Wang & Michael Z. Lin & Wei Wei, 2024. "Dendritic mGluR2 and perisomatic Kv3 signaling regulate dendritic computation of mouse starburst amacrine cells," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    5. Yeon Jin Kim & Beth B. Peterson & Joanna D. Crook & Hannah R. Joo & Jiajia Wu & Christian Puller & Farrel R. Robinson & Paul D. Gamlin & King-Wai Yau & Felix Viana & John B. Troy & Robert G. Smith & O, 2022. "Origins of direction selectivity in the primate retina," Nature Communications, Nature, vol. 13(1), pages 1-20, December.

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