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Augmenting insect olfaction performance through nano-neuromodulation

Nature Nanotechnology (2024)Cite this article

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Abstract

Biological olfactory systems are highly sensitive and selective, often outperforming engineered chemical sensors in highly complex and dynamic environments. As a result, there is much interest in using biological systems to build sensors. However, approaches to read-out information from biological systems, especially neural signals, tend to be suboptimal due to the number of electrodes that can be used and where these can be placed. Here we aim to overcome this suboptimality in neural information read-out by using a nano-enabled neuromodulation strategy to augment insect olfaction-based chemical sensors. By harnessing the photothermal properties of nanostructures and releasing a select neuromodulator on demand, we show that the odour-evoked response from the interrogated regions of the insect olfactory system can not only be enhanced but can also improve odour identification.

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Fig. 1: Neuromodulation strategy for augmenting insect olfaction.
Fig. 2: Synthesis and characterization of photothermal NPs.
Fig. 3: Augmentation of locust olfaction via nanomaterial-assisted photothermal neuromodulation.
Fig. 4: Cargo loading and triggered release kinetics of nanovehicles.
Fig. 5: Effect of chemical neuromodulation on locust olfaction.
Fig. 6: Augmenting locust olfaction via nano-enabled synergistic photothermal/chemical neuromodulation.

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Data availability

The main data supporting the results in this study are available within the paper and the Supplementary Information. All data generated in this study are available from figshare via the identifier https://doi.org/10.6084/m9.figshare.24582537.

Code availability

The codes used for data analyses are available from figshare via the identifier https://doi.org/10.6084/m9.figshare.24582537.

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Acknowledgements

The authors acknowledge support from the Air Force Office of Scientific Research (#FA95501910394 (S.S. and B.R.)) and the Office of Naval Research (#N000142112343 (B.R., S.C. and S.S.)). The authors thank the Nano Research Facility (NRF) and the Institute of Materials Science and Engineering at Washington University for providing access to material characterization facilities. Parts of the schematic illustrations depicted in Figs. 1, 2j, 3a, 4a–c, 5a and 6a and Supplementary Figs. 9a and 27a were created in BioRender.com (agreement number KL265ATGEY) and assembled in Microsoft Powerpoint. We thank Y. Liu for his help with the BioRender images.

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Authors and Affiliations

  1. Department of Mechanical Engineering and Materials Science, and Institute of Materials Science and Engineering, Washington University in St Louis, St Louis, MO, USA

    Prashant Gupta, Avishek Debnath, Hamed Gholami Derami, Harsh Baldi & Srikanth Singamaneni

  2. Department of Biomedical Engineering, Washington University in St Louis, St Louis, MO, USA

    Rishabh Chandak, Michael Traner, Hengbo Huang & Baranidharan Raman

  3. Department of Emergency Medicine, Washington University School of Medicine, St Louis, MO, USA

    Brendan M. Watson

  4. Department of Radiology, Washington University School of Medicine, Washington University in St Louis, St Louis, MO, USA

    Hengbo Huang

  5. Department of Electrical & Systems Engineering, Washington University in St Louis, St Louis, MO, USA

    Shantanu Chakrabartty

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Contributions

S.S., B.R. and P.G. conceived the project. P.G., S.S., B.R. and S.C. designed the experiments. P.G. performed most of the experiments. P.G. synthesized the NPs with assistance from H.G.D. H.G.D. also assisted in the experiments related to triggered release of the dye in the insect brain. P.G. performed photothermally triggered cargo release kinetics of the NPs with assistance from H.H. and H.B. P.G. performed in vivo neural recordings with assistance from R.C. and M.T. R.C. assisted P.G. in neural data analysis. A.D. performed scanning electron microscopy of NPs. B.M.W. performed 1H NMR analysis of the released octopamine. P.G. wrote the first draft of the manuscript with input from S.S., B.R. and S.C. All authors read and commented on the manuscript.

Corresponding authors

Correspondence to Baranidharan Raman or Srikanth Singamaneni.

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Nature Nanotechnology thanks Michael Schmuker, Yao Li, and the other, anonymous, reviewer for their contribution to the peer review of this work.

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Supplementary Discussion 1–12 and Figs. 1–27.

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Gupta, P., Chandak, R., Debnath, A. et al. Augmenting insect olfaction performance through nano-neuromodulation. Nat. Nanotechnol. (2024). https://doi.org/10.1038/s41565-023-01592-z

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