IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40444-1.html
   My bibliography  Save this article

Stimulus edges induce orientation tuning in superior colliculus

Author

Listed:
  • Yajie Liang

    (Howard Hughes Medical Institute
    University of Maryland School of Medicine)

  • Rongwen Lu

    (Howard Hughes Medical Institute)

  • Katharine Borges

    (University of California)

  • Na Ji

    (Howard Hughes Medical Institute
    University of California
    University of California
    University of California)

Abstract

Orientation columns exist in the primary visual cortex (V1) of cat and primates but not mouse. Intriguingly, some recent studies reported the presence of orientation and direction columns in the mouse superficial superior colliculus (sSC), while others reported a lack of columnar organization therein. Using in vivo calcium imaging of sSC in the awake mouse brain, we found that the presence of columns is highly stimulus dependent. Specifically, we observed orientation and direction columns formed by sSC neurons retinotopically mapped to the edge of grating stimuli. For both excitatory and inhibitory neurons in sSC, orientation selectivity can be induced by the edge with their preferred orientation perpendicular to the edge orientation. Furthermore, we found that this edge-induced orientation selectivity is associated with saliency encoding. These findings indicate that the tuning properties of sSC neurons are not fixed by circuit architecture but rather dependent on the spatiotemporal properties of the stimulus.

Suggested Citation

  • Yajie Liang & Rongwen Lu & Katharine Borges & Na Ji, 2023. "Stimulus edges induce orientation tuning in superior colliculus," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40444-1
    DOI: 10.1038/s41467-023-40444-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40444-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-40444-1?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. Jonathan B. Levitt & Jennifer S. Lund, 1997. "Contrast dependence of contextual effects in primate visual cortex," Nature, Nature, vol. 387(6628), pages 73-76, May.
    2. Kenichi Ohki & Sooyoung Chung & Yeang H. Ch'ng & Prakash Kara & R. Clay Reid, 2005. "Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex," Nature, Nature, vol. 433(7026), pages 597-603, February.
    3. Mehran Ahmadlou & J Alexander Heimel, 2015. "Preference for concentric orientations in the mouse superior colliculus," Nature Communications, Nature, vol. 6(1), pages 1-11, November.
    4. Tom Baden & Philipp Berens & Katrin Franke & Miroslav Román Rosón & Matthias Bethge & Thomas Euler, 2016. "The functional diversity of retinal ganglion cells in the mouse," Nature, Nature, vol. 529(7586), pages 345-350, January.
    5. Amit Basole & Leonard E. White & David Fitzpatrick, 2003. "Mapping multiple features in the population response of visual cortex," Nature, Nature, vol. 423(6943), pages 986-990, June.
    6. James B. Ackman & Timothy J. Burbridge & Michael C. Crair, 2012. "Retinal waves coordinate patterned activity throughout the developing visual system," Nature, Nature, vol. 490(7419), pages 219-225, October.
    7. Pengfei Wei & Nan Liu & Zhijian Zhang & Xuemei Liu & Yongqiang Tang & Xiaobin He & Bifeng Wu & Zheng Zhou & Yaohan Liu & Juan Li & Yi Zhang & Xuanyi Zhou & Lin Xu & Lin Chen & Guoqiang Bi & Xintian Hu, 2015. "Processing of visually evoked innate fear by a non-canonical thalamic pathway," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    8. Jens Kremkow & Jianzhong Jin & Yushi Wang & Jose M. Alonso, 2016. "Principles underlying sensory map topography in primary visual cortex," Nature, Nature, vol. 533(7601), pages 52-57, May.
    9. Evan H. Feinberg & Markus Meister, 2015. "Orientation columns in the mouse superior colliculus," Nature, Nature, vol. 519(7542), pages 229-232, March.
    Full references (including those not matched with items on IDEAS)

    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. Jérémie Sibille & Carolin Gehr & Jonathan I. Benichov & Hymavathy Balasubramanian & Kai Lun Teh & Tatiana Lupashina & Daniela Vallentin & Jens Kremkow, 2022. "High-density electrode recordings reveal strong and specific connections between retinal ganglion cells and midbrain neurons," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Elaine Tring & Konnie K. Duan & Dario L. Ringach, 2022. "ON/OFF domains shape receptive field structure in mouse visual cortex," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    3. Dmitry Molotkov & Leiron Ferrarese & Tom Boissonnet & Hiroki Asari, 2023. "Topographic axonal projection at single-cell precision supports local retinotopy in the mouse superior colliculus," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    4. Li Zhaoping & Li Zhe, 2015. "Primary Visual Cortex as a Saliency Map: A Parameter-Free Prediction and Its Test by Behavioral Data," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-39, October.
    5. Ruben Coen-Cagli & Peter Dayan & Odelia Schwartz, 2012. "Cortical Surround Interactions and Perceptual Salience via Natural Scene Statistics," PLOS Computational Biology, Public Library of Science, vol. 8(3), pages 1-18, March.
    6. Lei Wang & Xin Liu & Yin Zhang, 2023. "A communication-efficient and privacy-aware distributed algorithm for sparse PCA," Computational Optimization and Applications, Springer, vol. 85(3), pages 1033-1072, July.
    7. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. 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.
    9. 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.
    10. Sohrab Najafian & Erin Koch & Kai Lun Teh & Jianzhong Jin & Hamed Rahimi-Nasrabadi & Qasim Zaidi & Jens Kremkow & Jose-Manuel Alonso, 2022. "A theory of cortical map formation in the visual brain," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    11. Ke Yang & Yanghao Wang & Pek Jun Tiw & Chaoming Wang & Xiaolong Zou & Rui Yuan & Chang Liu & Ge Li & Chen Ge & Si Wu & Teng Zhang & Ru Huang & Yuchao Yang, 2024. "High-order sensory processing nanocircuit based on coupled VO2 oscillators," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    12. 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.
    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. Qiang Sang & Biao Cai & Hao Chen, 2017. "Contour detection improved by context-adaptive surround suppression," PLOS ONE, Public Library of Science, vol. 12(7), pages 1-13, July.
    15. Yulin Shi & Zoran Nenadic & Xiangmin Xu, 2010. "Novel Use of Matched Filtering for Synaptic Event Detection and Extraction," PLOS ONE, Public Library of Science, vol. 5(11), pages 1-15, November.
    16. Lan Pang & Zhiguo Liu & Jiani Chen & Zhi Dong & Sicong Zhou & Qichao Zhang & Yueqi Lu & Yifeng Sheng & Xuexin Chen & Jianhua Huang, 2022. "Search performance and octopamine neuronal signaling mediate parasitoid induced changes in Drosophila oviposition behavior," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    17. 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.
    18. 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.
    19. 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.
    20. 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.

    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:14:y:2023:i:1:d:10.1038_s41467-023-40444-1. 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.