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Inhibition decorrelates visual feature representations in the inner retina

Author

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  • Katrin Franke

    (Centre for Integrative Neuroscience, University of Tübingen
    Bernstein Centre for Computational Neuroscience, University of Tübingen
    Institute for Ophthalmic Research, University of Tübingen
    Graduate School of Neural & Behavioural Sciences, International Max Planck Research School, University of Tübingen)

  • Philipp Berens

    (Centre for Integrative Neuroscience, University of Tübingen
    Bernstein Centre for Computational Neuroscience, University of Tübingen
    Institute for Ophthalmic Research, University of Tübingen)

  • Timm Schubert

    (Centre for Integrative Neuroscience, University of Tübingen
    Institute for Ophthalmic Research, University of Tübingen)

  • Matthias Bethge

    (Centre for Integrative Neuroscience, University of Tübingen
    Bernstein Centre for Computational Neuroscience, University of Tübingen
    Institute for Theoretical Physics, University of Tübingen
    Max Planck Institute of Biological Cybernetics)

  • Thomas Euler

    (Centre for Integrative Neuroscience, University of Tübingen
    Bernstein Centre for Computational Neuroscience, University of Tübingen
    Institute for Ophthalmic Research, University of Tübingen)

  • Tom Baden

    (Centre for Integrative Neuroscience, University of Tübingen
    Bernstein Centre for Computational Neuroscience, University of Tübingen
    Institute for Ophthalmic Research, University of Tübingen
    School of Life Sciences, University of Sussex)

Abstract

The retina extracts visual features for transmission to the brain. Different types of bipolar cell split the photoreceptor input into parallel channels and provide the excitatory drive for downstream visual circuits. Mouse bipolar cell types have been described at great anatomical and genetic detail, but a similarly deep understanding of their functional diversity is lacking. Here, by imaging light-driven glutamate release from more than 13,000 bipolar cell axon terminals in the intact retina, we show that bipolar cell functional diversity is generated by the interplay of dendritic excitatory inputs and axonal inhibitory inputs. The resulting centre and surround components of bipolar cell receptive fields interact to decorrelate bipolar cell output in the spatial and temporal domains. Our findings highlight the importance of inhibitory circuits in generating functionally diverse excitatory pathways and suggest that decorrelation of parallel visual pathways begins as early as the second synapse of the mouse visual system.

Suggested Citation

  • Katrin Franke & Philipp Berens & Timm Schubert & Matthias Bethge & Thomas Euler & Tom Baden, 2017. "Inhibition decorrelates visual feature representations in the inner retina," Nature, Nature, vol. 542(7642), pages 439-444, February.
    • Handle: RePEc:nat:nature:v:542:y:2017:i:7642:d:10.1038_nature21394
    DOI: 10.1038/nature21394
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    Citations

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    Cited by:

    1. Toshiyuki Ishii & Toshihiko Hosoya, 2020. "Interspike intervals within retinal spike bursts combinatorially encode multiple stimulus features," PLOS Computational Biology, Public Library of Science, vol. 16(11), pages 1-30, November.
    2. 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.
    3. Niru Maheswaranathan & David B Kastner & Stephen A Baccus & Surya Ganguli, 2018. "Inferring hidden structure in multilayered neural circuits," PLOS Computational Biology, Public Library of Science, vol. 14(8), pages 1-30, August.
    4. Chad P. Grabner & Daiki Futagi & Jun Shi & Vytas Bindokas & Katsunori Kitano & Eric A. Schwartz & Steven H. DeVries, 2023. "Mechanisms of simultaneous linear and nonlinear computations at the mammalian cone photoreceptor synapse," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Jacqueline Cornean & Sebastian Molina-Obando & Burak Gür & Annika Bast & Giordano Ramos-Traslosheros & Jonas Chojetzki & Lena Lörsch & Maria Ioannidou & Rachita Taneja & Christopher Schnaitmann & Mari, 2024. "Heterogeneity of synaptic connectivity in the fly visual system," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. Luke E Rogerson & Zhijian Zhao & Katrin Franke & Thomas Euler & Philipp Berens, 2019. "Bayesian hypothesis testing and experimental design for two-photon imaging data," PLOS Computational Biology, Public Library of Science, vol. 15(8), pages 1-27, August.
    7. David Swygart & Wan-Qing Yu & Shunsuke Takeuchi & Rachel O. L. Wong & Gregory W. Schwartz, 2024. "A presynaptic source drives differing levels of surround suppression in two mouse retinal ganglion cell types," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    8. Andrew Jo & Sercan Deniz & Jian Xu & Robert M. Duvoisin & Steven H. DeVries & Yongling Zhu, 2023. "A sign-inverted receptive field of inhibitory interneurons provides a pathway for ON-OFF interactions in the retina," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. 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.
    10. Jen-Chun Hsiang & Ning Shen & Florentina Soto & Daniel Kerschensteiner, 2024. "Distributed feature representations of natural stimuli across parallel retinal pathways," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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