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Non-synaptic inhibition between grouped neurons in an olfactory circuit

Abstract

Diverse sensory organs, including mammalian taste buds and insect chemosensory sensilla, show a marked compartmentalization of receptor cells; however, the functional impact of this organization remains unclear. Here we show that compartmentalized Drosophila olfactory receptor neurons (ORNs) communicate with each other directly. The sustained response of one ORN is inhibited by the transient activation of a neighbouring ORN. Mechanistically, such lateral inhibition does not depend on synapses and is probably mediated by ephaptic coupling. Moreover, lateral inhibition in the periphery can modulate olfactory behaviour. Together, the results show that integration of olfactory information can occur via lateral interactions between ORNs. Inhibition of a sustained response by a transient response may provide a means of encoding salience. Finally, a CO2-sensitive ORN in the malaria mosquito Anopheles can also be inhibited by excitation of an adjacent ORN, suggesting a broad occurrence of lateral inhibition in insects and possible applications in insect control.

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Figure 1: Lateral inhibition of ORNs.
Figure 2: Lateral inhibition in diverse sensilla.
Figure 3: Lateral inhibition is dose-dependent.
Figure 4: Lateral inhibition does not require synapses.
Figure 5: Lateral inhibition modulates behaviour.

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Acknowledgements

We thank J. Cardin for help with establishing the optogenetics system; Y. Zhao and E. Fikrig for providing mosquitoes; A. Tzingounis and G. Lowe for suggestions; Z. Berman and P. Graham for technical assistance; T. Koh for suggestions and for sharing reagents; and G. Thomas, F. Marion-Poll, R. Wyman and D. McCormick for comments on the manuscript. This work was funded by National Institutes of Health (NIH) grants to J.R.C. and by a grant from the Foundation for the NIH through the Grand Challenges in Global Health Initiative (GCGH no. 121); an NRSA postdoctoral fellowship to K.M. (NIH F32DC011242); and an NIH grant to J.R. (NIH DC009613).

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C.-Y.S. designed, performed the experiments and analysed the data, except for coeloconic sensillum recordings and cross-correlation analysis, which were performed by K.M. and J.R., respectively. The model was elaborated primarily by K.M. C.-Y.S., K.M. and J.R.C. wrote the manuscript. All authors contributed to the interpretation of the study.

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Correspondence to John R. Carlson.

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The authors declare no competing financial interests.

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Su, CY., Menuz, K., Reisert, J. et al. Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 492, 66–71 (2012). https://doi.org/10.1038/nature11712

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