IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-32761-8.html
   My bibliography  Save this article

Classical center-surround receptive fields facilitate novel object detection in retinal bipolar cells

Author

Listed:
  • John A. Gaynes

    (University of Colorado School of Medicine)

  • Samuel A. Budoff

    (University of Colorado School of Medicine)

  • Michael J. Grybko

    (University of Colorado School of Medicine)

  • Joshua B. Hunt

    (University of Colorado School of Medicine)

  • Alon Poleg-Polsky

    (University of Colorado School of Medicine)

Abstract

Antagonistic interactions between center and surround receptive field (RF) components lie at the heart of the computations performed in the visual system. Circularly symmetric center-surround RFs are thought to enhance responses to spatial contrasts (i.e., edges), but how visual edges affect motion processing is unclear. Here, we addressed this question in retinal bipolar cells, the first visual neuron with classic center-surround interactions. We found that bipolar glutamate release emphasizes objects that emerge in the RF; their responses to continuous motion are smaller, slower, and cannot be predicted by signals elicited by stationary stimuli. In our hands, the alteration in signal dynamics induced by novel objects was more pronounced than edge enhancement and could be explained by priming of RF surround during continuous motion. These findings echo the salience of human visual perception and demonstrate an unappreciated capacity of the center-surround architecture to facilitate novel object detection and dynamic signal representation.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32761-8
    DOI: 10.1038/s41467-022-32761-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-32761-8
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-32761-8?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Michael J. Berry & Iman H. Brivanlou & Thomas A. Jordan & Markus Meister, 1999. "Anticipation of moving stimuli by the retina," Nature, Nature, vol. 398(6725), pages 334-338, March.
    2. Felice A. Dunn & Martin J. Lankheet & Fred Rieke, 2007. "Light adaptation in cone vision involves switching between receptor and post-receptor sites," Nature, Nature, vol. 449(7162), pages 603-606, October.
    3. 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.
    4. In-Jung Kim & Yifeng Zhang & Masahito Yamagata & Markus Meister & Joshua R. Sanes, 2008. "Molecular identification of a retinal cell type that responds to upward motion," Nature, Nature, vol. 452(7186), pages 478-482, March.
    5. 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.
    6. Xiaolin Huang & Melissa Rangel & Kevin L. Briggman & Wei Wei, 2019. "Neural mechanisms of contextual modulation in the retinal direction selective circuit," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    7. Bence P. Ölveczky & Stephen A. Baccus & Markus Meister, 2003. "Segregation of object and background motion in the retina," Nature, Nature, vol. 423(6938), pages 401-408, May.
    8. Huayu Ding & Robert G. Smith & Alon Poleg-Polsky & Jeffrey S. Diamond & Kevin L. Briggman, 2016. "Species-specific wiring for direction selectivity in the mammalian retina," Nature, Nature, vol. 535(7610), pages 105-110, July.
    9. Sarah Strauss & Maria M. Korympidou & Yanli Ran & Katrin Franke & Timm Schubert & Tom Baden & Philipp Berens & Thomas Euler & Anna L. Vlasits, 2022. "Center-surround interactions underlie bipolar cell motion sensitivity in the mouse retina," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Andrew Jo & Sercan Deniz & Suraj Cherian & Jian Xu & Daiki Futagi & Steven H. DeVries & Yongling Zhu, 2023. "Modular interneuron circuits control motion sensitivity in the mouse retina," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.
    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. 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.
    5. 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.
    6. 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.
    7. Matteo Saponati & Martin Vinck, 2023. "Sequence anticipation and spike-timing-dependent plasticity emerge from a predictive learning rule," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Donald R Cantrell & Jianhua Cang & John B Troy & Xiaorong Liu, 2010. "Non-Centered Spike-Triggered Covariance Analysis Reveals Neurotrophin-3 as a Developmental Regulator of Receptive Field Properties of ON-OFF Retinal Ganglion Cells," PLOS Computational Biology, Public Library of Science, vol. 6(10), pages 1-16, October.
    9. Mina A Khoei & Guillaume S Masson & Laurent U Perrinet, 2017. "The Flash-Lag Effect as a Motion-Based Predictive Shift," PLOS Computational Biology, Public Library of Science, vol. 13(1), pages 1-31, January.
    10. Pei-Yu Huang & Bi-Yi Jiang & Hong-Ji Chen & Jia-Yi Xu & Kang Wang & Cheng-Yi Zhu & Xin-Yan Hu & Dong Li & Liang Zhen & Fei-Chi Zhou & Jing-Kai Qin & Cheng-Yan Xu, 2023. "Neuro-inspired optical sensor array for high-accuracy static image recognition and dynamic trace extraction," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    11. 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.
    12. 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.
    13. Andrew Jo & Sercan Deniz & Suraj Cherian & Jian Xu & Daiki Futagi & Steven H. DeVries & Yongling Zhu, 2023. "Modular interneuron circuits control motion sensitivity in the mouse retina," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. 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.
    15. Gabriel D Puccini & Maria V Sanchez-Vives & Albert Compte, 2007. "Integrated Mechanisms of Anticipation and Rate-of-Change Computations in Cortical Circuits," PLOS Computational Biology, Public Library of Science, vol. 3(5), pages 1-13, May.
    16. Weston Cox & Brian J Fischer, 2015. "Optimal Prediction of Moving Sound Source Direction in the Owl," PLOS Computational Biology, Public Library of Science, vol. 11(7), pages 1-20, July.
    17. 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.
    18. Carles Bosch & Tobias Ackels & Alexandra Pacureanu & Yuxin Zhang & Christopher J. Peddie & Manuel Berning & Norman Rzepka & Marie-Christine Zdora & Isabell Whiteley & Malte Storm & Anne Bonnin & Chris, 2022. "Functional and multiscale 3D structural investigation of brain tissue through correlative in vivo physiology, synchrotron microtomography and volume electron microscopy," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    19. 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.
    20. Andrea Pintimalli & Joseph Glicksohn & Fabio Marson & Tania Di Giuseppe & Tal Dotan Ben-Soussan, 2023. "Change in Time Perception Following the Place of Pre-Existence Technique," IJERPH, MDPI, vol. 20(4), pages 1-19, February.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32761-8. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.