IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42613-8.html
   My bibliography  Save this article

Sensorimotor transformation underlying odor-modulated locomotion in walking Drosophila

Author

Listed:
  • Liangyu Tao

    (Drexel University)

  • Samuel P. Wechsler

    (Drexel University
    Drexel University)

  • Vikas Bhandawat

    (Drexel University)

Abstract

Most real-world behaviors – such as odor-guided locomotion - are performed with incomplete information. Activity in olfactory receptor neuron (ORN) classes provides information about odor identity but not the location of its source. In this study, we investigate the sensorimotor transformation that relates ORN activation to locomotion changes in Drosophila by optogenetically activating different combinations of ORN classes and measuring the resulting changes in locomotion. Three features describe this sensorimotor transformation: First, locomotion depends on both the instantaneous firing frequency (f) and its change (df); the two together serve as a short-term memory that allows the fly to adapt its motor program to sensory context automatically. Second, the mapping between (f, df) and locomotor parameters such as speed or curvature is distinct for each pattern of activated ORNs. Finally, the sensorimotor mapping changes with time after odor exposure, allowing information integration over a longer timescale.

Suggested Citation

  • Liangyu Tao & Samuel P. Wechsler & Vikas Bhandawat, 2023. "Sensorimotor transformation underlying odor-modulated locomotion in walking Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42613-8
    DOI: 10.1038/s41467-023-42613-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42613-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-42613-8?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. Liangyu Tao & Siddhi Ozarkar & Vikas Bhandawat, 2020. "Mechanisms underlying attraction to odors in walking Drosophila," PLOS Computational Biology, Public Library of Science, vol. 16(3), pages 1-26, March.
    2. Julia L. Semmelhack & Jing W. Wang, 2009. "Select Drosophila glomeruli mediate innate olfactory attraction and aversion," Nature, Nature, vol. 459(7244), pages 218-223, May.
    3. Quentin Gaudry & Elizabeth J. Hong & Jamey Kain & Benjamin L. de Bivort & Rachel I. Wilson, 2013. "Asymmetric neurotransmitter release enables rapid odour lateralization in Drosophila," Nature, Nature, vol. 493(7432), pages 424-428, January.
    4. Hernandez-Nunez, Luis & Jonas Belina & Mason Klein & Si, Guangwei & Lindsey Claus & John R. Carlson & Aravinthan D T Samuel, 2015. "Reverse-correlation analysis of navigation dynamics in Drosophila larva using optogenetics," Working Paper 251296, Harvard University OpenScholar.
    5. Minrong Ai & Soohong Min & Yael Grosjean & Charlotte Leblanc & Rati Bell & Richard Benton & Greg S. B. Suh, 2010. "Acid sensing by the Drosophila olfactory system," Nature, Nature, vol. 468(7324), pages 691-695, December.
    6. Hernandez-Nunez, Luis & Jonas Belina & Mason Klein & Si, Guangwei & Lindsey Claus & John R. Carlson & Aravinthan D T Samuel, 2015. "Reverse-correlation analysis of navigation dynamics in Drosophila larva using optogenetics," Working Paper 251291, Harvard University OpenScholar.
    7. Alex Gomez-Marin & Greg J. Stephens & Matthieu Louis, 2011. "Active sampling and decision making in Drosophila chemotaxis," Nature Communications, Nature, vol. 2(1), pages 1-10, September.
    8. Jonathan W. Pillow & Jonathon Shlens & Liam Paninski & Alexander Sher & Alan M. Litke & E. J. Chichilnisky & Eero P. Simoncelli, 2008. "Spatio-temporal correlations and visual signalling in a complete neuronal population," Nature, Nature, vol. 454(7207), pages 995-999, August.
    9. Nirag Kadakia & Mahmut Demir & Brenden T. Michaelis & Brian D. DeAngelis & Matthew A. Reidenbach & Damon A. Clark & Thierry Emonet, 2022. "Odour motion sensing enhances navigation of complex plumes," Nature, Nature, vol. 611(7937), pages 754-761, November.
    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. Liangyu Tao & Siddhi Ozarkar & Vikas Bhandawat, 2020. "Mechanisms underlying attraction to odors in walking Drosophila," PLOS Computational Biology, Public Library of Science, vol. 16(3), pages 1-26, March.
    2. Arne F Meyer & Jan-Philipp Diepenbrock & Max F K Happel & Frank W Ohl & Jörn Anemüller, 2014. "Discriminative Learning of Receptive Fields from Responses to Non-Gaussian Stimulus Ensembles," PLOS ONE, Public Library of Science, vol. 9(4), pages 1-15, April.
    3. Jonathan Rubin & Nachum Ulanovsky & Israel Nelken & Naftali Tishby, 2016. "The Representation of Prediction Error in Auditory Cortex," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-28, August.
    4. Franklin Leong & Babak Rahmani & Demetri Psaltis & Christophe Moser & Diego Ghezzi, 2024. "An actor-model framework for visual sensory encoding," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Lucas Rudelt & Daniel González Marx & Michael Wibral & Viola Priesemann, 2021. "Embedding optimization reveals long-lasting history dependence in neural spiking activity," PLOS Computational Biology, Public Library of Science, vol. 17(6), pages 1-51, June.
    6. Pengcheng Zhou & Shawn D Burton & Adam C Snyder & Matthew A Smith & Nathaniel N Urban & Robert E Kass, 2015. "Establishing a Statistical Link between Network Oscillations and Neural Synchrony," PLOS Computational Biology, Public Library of Science, vol. 11(10), pages 1-25, October.
    7. Richard Naud & Wulfram Gerstner, 2012. "Coding and Decoding with Adapting Neurons: A Population Approach to the Peri-Stimulus Time Histogram," PLOS Computational Biology, Public Library of Science, vol. 8(10), pages 1-14, October.
    8. Fanfan Li & Dingwei Li & Chuanqing Wang & Guolei Liu & Rui Wang & Huihui Ren & Yingjie Tang & Yan Wang & Yitong Chen & Kun Liang & Qi Huang & Mohamad Sawan & Min Qiu & Hong Wang & Bowen Zhu, 2024. "An artificial visual neuron with multiplexed rate and time-to-first-spike coding," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    9. Kenneth W. Latimer & David J. Freedman, 2023. "Low-dimensional encoding of decisions in parietal cortex reflects long-term training history," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    10. Javier J How & Saket Navlakha & Sreekanth H Chalasani, 2021. "Neural network features distinguish chemosensory stimuli in Caenorhabditis elegans," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-38, November.
    11. Braden A W Brinkman & Alison I Weber & Fred Rieke & Eric Shea-Brown, 2016. "How Do Efficient Coding Strategies Depend on Origins of Noise in Neural Circuits?," PLOS Computational Biology, Public Library of Science, vol. 12(10), pages 1-34, October.
    12. 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.
    13. Yanyun Ren & Xiaobo Bu & Ming Wang & Yue Gong & Junjie Wang & Yuyang Yang & Guijun Li & Meng Zhang & Ye Zhou & Su-Ting Han, 2022. "Synaptic plasticity in self-powered artificial striate cortex for binocular orientation selectivity," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    14. Jan Humplik & Gašper Tkačik, 2017. "Probabilistic models for neural populations that naturally capture global coupling and criticality," PLOS Computational Biology, Public Library of Science, vol. 13(9), pages 1-26, September.
    15. Anirban Das & Alec G. Sheffield & Anirvan S. Nandy & Monika P. Jadi, 2024. "Brain-state mediated modulation of inter-laminar dependencies in visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    16. Urs Köster & Jascha Sohl-Dickstein & Charles M Gray & Bruno A Olshausen, 2014. "Modeling Higher-Order Correlations within Cortical Microcolumns," PLOS Computational Biology, Public Library of Science, vol. 10(7), pages 1-12, July.
    17. 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.
    18. Philip A. White & Alan E. Gelfand, 2021. "Generalized Evolutionary Point Processes: Model Specifications and Model Comparison," Methodology and Computing in Applied Probability, Springer, vol. 23(3), pages 1001-1021, September.
    19. Michael E Rule & David Schnoerr & Matthias H Hennig & Guido Sanguinetti, 2019. "Neural field models for latent state inference: Application to large-scale neuronal recordings," PLOS Computational Biology, Public Library of Science, vol. 15(11), pages 1-23, November.
    20. Martin J M Lankheet & P Christiaan Klink & Bart G Borghuis & André J Noest, 2012. "Spike-Interval Triggered Averaging Reveals a Quasi-Periodic Spiking Alternative for Stochastic Resonance in Catfish Electroreceptors," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-11, March.

    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_s41467-023-42613-8. 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.