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Fast odour dynamics are encoded in the olfactory system and guide behaviour

Author

Listed:
  • Tobias Ackels

    (The Francis Crick Institute
    University College London)

  • Andrew Erskine

    (The Francis Crick Institute
    University College London)

  • Debanjan Dasgupta

    (The Francis Crick Institute
    University College London)

  • Alina Cristina Marin

    (The Francis Crick Institute)

  • Tom P. A. Warner

    (The Francis Crick Institute)

  • Sina Tootoonian

    (The Francis Crick Institute
    University College London)

  • Izumi Fukunaga

    (The Francis Crick Institute)

  • Julia J. Harris

    (The Francis Crick Institute
    University College London)

  • Andreas T. Schaefer

    (The Francis Crick Institute
    University College London)

Abstract

Odours are transported in turbulent plumes, which result in rapid concentration fluctuations1,2 that contain rich information about the olfactory scenery, such as the composition and location of an odour source2–4. However, it is unclear whether the mammalian olfactory system can use the underlying temporal structure to extract information about the environment. Here we show that ten-millisecond odour pulse patterns produce distinct responses in olfactory receptor neurons. In operant conditioning experiments, mice discriminated temporal correlations of rapidly fluctuating odours at frequencies of up to 40 Hz. In imaging and electrophysiological recordings, such correlation information could be readily extracted from the activity of mitral and tufted cells—the output neurons of the olfactory bulb. Furthermore, temporal correlation of odour concentrations5 reliably predicted whether odorants emerged from the same or different sources in naturalistic environments with complex airflow. Experiments in which mice were trained on such tasks and probed using synthetic correlated stimuli at different frequencies suggest that mice can use the temporal structure of odours to extract information about space. Thus, the mammalian olfactory system has access to unexpectedly fast temporal features in odour stimuli. This endows animals with the capacity to overcome key behavioural challenges such as odour source separation5, figure–ground segregation6 and odour localization7 by extracting information about space from temporal odour dynamics.

Suggested Citation

  • Tobias Ackels & Andrew Erskine & Debanjan Dasgupta & Alina Cristina Marin & Tom P. A. Warner & Sina Tootoonian & Izumi Fukunaga & Julia J. Harris & Andreas T. Schaefer, 2021. "Fast odour dynamics are encoded in the olfactory system and guide behaviour," Nature, Nature, vol. 593(7860), pages 558-563, May.
  • Handle: RePEc:nat:nature:v:593:y:2021:i:7860:d:10.1038_s41586-021-03514-2
    DOI: 10.1038/s41586-021-03514-2
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    Cited by:

    1. 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.
    2. Samuel K. H. Sy & Danny C. W. Chan & Roy C. H. Chan & Jing Lyu & Zhongqi Li & Kenneth K. Y. Wong & Chung Hang Jonathan Choi & Vincent C. T. Mok & Hei-Ming Lai & Owen Randlett & Yu Hu & Ho Ko, 2023. "An optofluidic platform for interrogating chemosensory behavior and brainwide neural representation in larval zebrafish," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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