IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43566-8.html
   My bibliography  Save this article

Different spectral sensitivities of ON- and OFF-motion pathways enhance the detection of approaching color objects in Drosophila

Author

Listed:
  • Kit D. Longden

    (HHMI Janelia Research Campus)

  • Edward M. Rogers

    (HHMI Janelia Research Campus)

  • Aljoscha Nern

    (HHMI Janelia Research Campus)

  • Heather Dionne

    (HHMI Janelia Research Campus)

  • Michael B. Reiser

    (HHMI Janelia Research Campus)

Abstract

Color and motion are used by many species to identify salient objects. They are processed largely independently, but color contributes to motion processing in humans, for example, enabling moving colored objects to be detected when their luminance matches the background. Here, we demonstrate an unexpected, additional contribution of color to motion vision in Drosophila. We show that behavioral ON-motion responses are more sensitive to UV than for OFF-motion, and we identify cellular pathways connecting UV-sensitive R7 photoreceptors to ON and OFF-motion-sensitive T4 and T5 cells, using neurogenetics and calcium imaging. Remarkably, this contribution of color circuitry to motion vision enhances the detection of approaching UV discs, but not green discs with the same chromatic contrast, and we show how this could generalize for systems with ON- and OFF-motion pathways. Our results provide a computational and circuit basis for how color enhances motion vision to favor the detection of saliently colored objects.

Suggested Citation

  • Kit D. Longden & Edward M. Rogers & Aljoscha Nern & Heather Dionne & Michael B. Reiser, 2023. "Different spectral sensitivities of ON- and OFF-motion pathways enhance the detection of approaching color objects in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43566-8
    DOI: 10.1038/s41467-023-43566-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43566-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-43566-8?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. Shin-ya Takemura & Arjun Bharioke & Zhiyuan Lu & Aljoscha Nern & Shiv Vitaladevuni & Patricia K. Rivlin & William T. Katz & Donald J. Olbris & Stephen M. Plaza & Philip Winston & Ting Zhao & Jane Anne, 2013. "A visual motion detection circuit suggested by Drosophila connectomics," Nature, Nature, vol. 500(7461), pages 175-181, August.
    2. Maximilian Joesch & Bettina Schnell & Shamprasad Varija Raghu & Dierk F. Reiff & Alexander Borst, 2010. "ON and OFF pathways in Drosophila motion vision," Nature, Nature, vol. 468(7321), pages 300-304, November.
    3. Klaudia P. Szatko & Maria M. Korympidou & Yanli Ran & Philipp Berens & Deniz Dalkara & Timm Schubert & Thomas Euler & Katrin Franke, 2020. "Neural circuits in the mouse retina support color vision in the upper visual field," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    4. Giordano Ramos-Traslosheros & Marion Silies, 2021. "The physiological basis for contrast opponency in motion computation in Drosophila," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    5. Nathan C. Klapoetke & Aljoscha Nern & Martin Y. Peek & Edward M. Rogers & Patrick Breads & Gerald M. Rubin & Michael B. Reiser & Gwyneth M. Card, 2017. "Ultra-selective looming detection from radial motion opponency," Nature, Nature, vol. 551(7679), pages 237-241, November.
    6. Matthew S. Maisak & Juergen Haag & Georg Ammer & Etienne Serbe & Matthias Meier & Aljoscha Leonhardt & Tabea Schilling & Armin Bahl & Gerald M. Rubin & Aljoscha Nern & Barry J. Dickson & Dierk F. Reif, 2013. "A directional tuning map of Drosophila elementary motion detectors," Nature, Nature, vol. 500(7461), pages 212-216, August.
    7. Fumika N. Hamada & Mark Rosenzweig & Kyeongjin Kang & Stefan R. Pulver & Alfredo Ghezzi & Timothy J. Jegla & Paul A. Garrity, 2008. "An internal thermal sensor controlling temperature preference in Drosophila," Nature, Nature, vol. 454(7201), pages 217-220, July.
    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. Burak Gür & Luisa Ramirez & Jacqueline Cornean & Freya Thurn & Sebastian Molina-Obando & Giordano Ramos-Traslosheros & Marion Silies, 2024. "Neural pathways and computations that achieve stable contrast processing tuned to natural scenes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. 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.
    3. Toufiq Parag & Anirban Chakraborty & Stephen Plaza & Louis Scheffer, 2015. "A Context-Aware Delayed Agglomeration Framework for Electron Microscopy Segmentation," PLOS ONE, Public Library of Science, vol. 10(5), pages 1-19, May.
    4. Daniel Soudry & Suraj Keshri & Patrick Stinson & Min-hwan Oh & Garud Iyengar & Liam Paninski, 2015. "Efficient "Shotgun" Inference of Neural Connectivity from Highly Sub-sampled Activity Data," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-30, October.
    5. Shang, Ke-ke & Small, Michael & Yan, Wei-sheng, 2017. "Link direction for link prediction," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 469(C), pages 767-776.
    6. Antoine Allard & M Ángeles Serrano, 2020. "Navigable maps of structural brain networks across species," PLOS Computational Biology, Public Library of Science, vol. 16(2), pages 1-20, February.
    7. Yue Yang & Fangduo Zhu & Xumeng Zhang & Pei Chen & Yongzhou Wang & Jiaxue Zhu & Yanting Ding & Lingli Cheng & Chao Li & Hao Jiang & Zhongrui Wang & Peng Lin & Tuo Shi & Ming Wang & Qi Liu & Ningsheng , 2024. "Firing feature-driven neural circuits with scalable memristive neurons for robotic obstacle avoidance," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    8. Andrea Censi & Andrew D Straw & Rosalyn W Sayaman & Richard M Murray & Michael H Dickinson, 2013. "Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila," PLOS Computational Biology, Public Library of Science, vol. 9(2), pages 1-14, February.
    9. 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.
    10. Junjun Gao & Song Zhang & Pan Deng & Zhigang Wu & Bruno Lemaitre & Zongzhao Zhai & Zheng Guo, 2024. "Dietary L-Glu sensing by enteroendocrine cells adjusts food intake via modulating gut PYY/NPF secretion," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    11. 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.
    12. Chen Zhang & Anmo J. Kim & Crisalesandra Rivera-Perez & Fernando G. Noriega & Young-Joon Kim, 2022. "The insect somatostatin pathway gates vitellogenesis progression during reproductive maturation and the post-mating response," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    13. Di Peng & Liubin Zheng & Dan Liu & Cheng Han & Xin Wang & Yan Yang & Li Song & Miaoying Zhao & Yanfeng Wei & Jiayi Li & Xiaoxue Ye & Yuxiang Wei & Zihao Feng & Xinhe Huang & Miaomiao Chen & Yujie Gou , 2024. "Large-language models facilitate discovery of the molecular signatures regulating sleep and activity," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Olga Kubrak & Takashi Koyama & Nadja Ahrentløv & Line Jensen & Alina Malita & Muhammad T. Naseem & Mette Lassen & Stanislav Nagy & Michael J. Texada & Kenneth V. Halberg & Kim Rewitz, 2022. "The gut hormone Allatostatin C/Somatostatin regulates food intake and metabolic homeostasis under nutrient stress," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    15. Shuman Huang & Xiaoke Niu & Zhizhong Wang & Gang Liu & Li Shi, 2023. "A Moving Target Detection Model Inspired by Spatio-Temporal Information Accumulation of Avian Tectal Neurons," Mathematics, MDPI, vol. 11(5), pages 1-18, February.
    16. Xiangjing Wang & Chunsheng Chen & Li Zhu & Kailu Shi & Baocheng Peng & Yixin Zhu & Huiwu Mao & Haotian Long & Shuo Ke & Chuanyu Fu & Ying Zhu & Changjin Wan & Qing Wan, 2023. "Vertically integrated spiking cone photoreceptor arrays for color perception," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    17. 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.
    18. Saha, Papri & Sarkar, Debasish, 2022. "Allometric scaling of von Neumann entropy in animal connectomes and its evolutionary aspect," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 600(C).
    19. Olga Kubrak & Anne F. Jørgensen & Takashi Koyama & Mette Lassen & Stanislav Nagy & Jacob Hald & Gianluca Mazzoni & Dennis Madsen & Jacob B. Hansen & Martin Røssel Larsen & Michael J. Texada & Jakob L., 2024. "LGR signaling mediates muscle-adipose tissue crosstalk and protects against diet-induced insulin resistance," Nature Communications, Nature, vol. 15(1), pages 1-22, 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_s41467-023-43566-8. 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.