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Decomposition of an odorant in olfactory perception and neural representation

Nature Human Behaviour (2024)Cite this article

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Abstract

Molecules—the elementary units of substances—are commonly considered the units of processing in olfactory perception, giving rise to undifferentiated odour objects invariant to environmental variations. By selectively perturbing the processing of chemical substructures with adaptation (‘the psychologist’s microelectrode’) in a series of psychophysical and neuroimaging experiments (458 participants), we show that two perceptually distinct odorants sharing part of their structural features become significantly less discernible following adaptation to a third odorant containing their non-shared structural features, in manners independent of olfactory intensity, valence, quality or general olfactory adaptation. The effect is accompanied by reorganizations of ensemble activity patterns in the posterior piriform cortex that parallel subjective odour quality changes, in addition to substructure-based neural adaptations in the anterior piriform cortex and amygdala. Central representations of odour quality and the perceptual outcome thus embed submolecular structural information and are malleable by recent olfactory encounters.

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Fig. 1: Behavioural assessments of substructure–quality relationship.
Fig. 2: Nostril-specific modulation of odour perception by substructure adaptation.
Fig. 3: Substructure-related neural adaptations.
Fig. 4: Selective reorganization of posterior piriform activity pattern following substructure adaptation.

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Data availability

All reported data are available at https://doi.org/10.57760/sciencedb.13818. Source data are provided with this paper.

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All analysis scripts are available at https://doi.org/10.57760/sciencedb.13818.

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Acknowledgements

We thank Q. Liu and X. Chang for assistance. This work was supported by STI2030-Major Projects 2021ZD0204200 (W.Z.); the Chinese Academy of Sciences grant nos. JCTD-2021-06 (W.Z.), 2021091 (Z.Z.) and YSBR-068 (Z.Z.); and the National Natural Science Foundation of China grant nos. 31830037 (W.Z.) and 32000789 (Y.Y.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Author information

Author notes

  1. These authors contributed equally: Yuting Ye, Yanqing Wang.

Authors and Affiliations

  1. State Key Laboratory of Brain and Cognitive Science, Institute of Psychology, Chinese Academy of Sciences, Beijing, China

    Yuting Ye, Yanqing Wang, Yuan Zhuang, Huibang Tan, Hanqi Yun, Kaiqi Yuan & Wen Zhou

  2. Department of Psychology, University of Chinese Academy of Sciences, Beijing, China

    Yuting Ye, Yanqing Wang, Yuan Zhuang, Huibang Tan, Hanqi Yun, Kaiqi Yuan & Wen Zhou

  3. Institute of Psychology, School of Public Affairs, Xiamen University, Xiamen, China

    Yuting Ye

  4. School of Psychology, Northwest Normal University, Lanzhou, China

    Yanqing Wang

  5. State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China

    Zhentao Zuo

  6. Institute of Artificial Intelligence, Hefei Comprehensive National Science Center, Hefei, China

    Zhentao Zuo

  7. Sino-Dannish College, University of Chinese Academy of Sciences, Beijing, China

    Zhentao Zuo

  8. Chinese Institute for Brain Research, Beijing, China

    Wen Zhou

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Contributions

W.Z. conceptualized the study. Y.Y., Y.W., Y.Z., H.T., H.Y. and K.Y. performed the experiments. Z.Z. optimized the imaging parameters. Y.Y., Y.W. and H.T. analysed the data under the supervision of W.Z. Y.Y., Y.W. and W.Z. wrote the manuscript.

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Correspondence to Wen Zhou.

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Nature Human Behaviour thanks Emilia Iannilli, Wen Li and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Ye, Y., Wang, Y., Zhuang, Y. et al. Decomposition of an odorant in olfactory perception and neural representation. Nat Hum Behav (2024). https://doi.org/10.1038/s41562-024-01849-0

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