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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.

References

  1. Su, C. Y., Menuz, K. & Carlson, J. R. Olfactory perception: receptors, cells, and circuits. Cell 139, 45–59 (2009)

    Article  CAS  Google Scholar 

  2. Shanbhag, S. R., Muller, B. & Steinbrecht, R. A. Atlas of olfactory organs of Drosophila melanogaster 1. Types, external organization, innervation and distribution of olfactory sensilla. Int. J. Insect Morphol. Embryol. 28, 377–397 (1999)

    Article  Google Scholar 

  3. Shanbhag, S. R., Muller, B. & Steinbrecht, R. A. Atlas of olfactory organs of Drosophila melanogaster 2. Internal organization and cellular architecture of olfactory sensilla. Arthropod Struct. Dev. 29, 211–229 (2000)

    Article  CAS  Google Scholar 

  4. Keil, T. A. Reconstruction and morphometry of silkmoth olfactory hairs: A comparative study of sensilla trichodea on the antennae of male Antheraea polyphemus and Antheraea pernyi (Insecta, Lepidoptera). Zoomorphology 104, 147–156 (1984)

    Article  Google Scholar 

  5. de Bruyne, M., Foster, K. & Carlson, J. R. Odor coding in the Drosophila antenna. Neuron 30, 537–552 (2001)

    Article  CAS  Google Scholar 

  6. Kaissling, K. E. Peripheral mechanisms of pheromone reception in moths. Chem. Senses 21, 257–268 (1996)

    Article  CAS  Google Scholar 

  7. Lu, T. et al. Odor coding in the maxillary palp of the malaria vector mosquito Anopheles gambiae. Curr. Biol. 17, 1533–1544 (2007)

    Article  CAS  Google Scholar 

  8. Akers, R. P. & O’Connell, R. J. The contribution of olfactory receptor neurons to the perception of pheromone component ratios in male redbanded leafroller moths. J. Comp. Physiol. A 163, 641–650 (1988)

    Article  CAS  Google Scholar 

  9. Takanashi, T. et al. Unusual response characteristics of pheromone-specific olfactory receptor neurons in the Asian corn borer moth, Ostrinia furnacalis. J. Exp. Biol. 209, 4946–4956 (2006)

    Article  CAS  Google Scholar 

  10. Hallem, E. A. & Carlson, J. R. Coding of odors by a receptor repertoire. Cell 125, 143–160 (2006)

    Article  CAS  Google Scholar 

  11. Couto, A., Alenius, M. & Dickson, B. J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535–1547 (2005)

    Article  CAS  Google Scholar 

  12. Suh, G. S. et al. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431, 854–859 (2004)

    Article  ADS  CAS  Google Scholar 

  13. Semmelhack, J. L. & Wang, J. W. Select Drosophila glomeruli mediate innate olfactory attraction and aversion. Nature 459, 218–223 (2009)

    Article  ADS  CAS  Google Scholar 

  14. Berg, B. G. & Mustaparta, H. The significance of major pheromone components and interspecific signals as expressed by receptor neurons in the oriental tobacco budworm moth, Helicoverpa assulta. J. Comp. Physiol. A 177, 683–694 (1995)

    CAS  Google Scholar 

  15. Nikonov, A. A. & Leal, W. S. Peripheral coding of sex pheromone and a behavioral antagonist in the Japanese beetle, Popillia japonica. J. Chem. Ecol. 28, 1075–1089 (2002)

    Article  CAS  Google Scholar 

  16. O’Connell, R. J. Responses to pheromone blends in insect olfactory receptor neurons. J. Comp. Physiol. A 156, 747–761 (1985)

    Article  MathSciNet  Google Scholar 

  17. Vermeulen, A. & Rospars, J. P. Why are insect olfactory receptor neurons grouped into sensilla? The teachings of a model investigating the effects of the electrical interaction between neurons on the transepithelial potential and the neuronal transmembrane potential. Eur. Biophys. J. 33, 633–643 (2004)

    Article  Google Scholar 

  18. Mitchell, B. K. Interactions of alkaloids with galeal chemosensory cells of Colorado potato beetle. J. Chem. Ecol. 13, 2009–2022 (1987)

    Article  CAS  Google Scholar 

  19. Schoonhoven, L. M. & Van Loon, J. J. A. An inventory of taste in caterpillars: each species its own key. Acta Zool. Hung. 48 (suppl. 1). 215–263 (2002)

    Google Scholar 

  20. Jorgensen, K., Almaas, T. J., Marion-Poll, F. & Mustaparta, H. Electrophysiological characterization of responses from gustatory receptor neurons of sensilla chaetica in the moth Heliothis virescens. Chem. Senses 32, 863–879 (2007)

    Article  Google Scholar 

  21. de Brito Sanchez, M. G., Giurfa, M., de Paula Mota, T. R. & Gauthier, M. Electrophysiological and behavioural characterization of gustatory responses to antennal ‘bitter’ taste in honeybees. Eur. J. Neurosci. 22, 3161–3170 (2005)

    Article  Google Scholar 

  22. Dethier, V. G. & Bowdan, E. The effect of alkaloids on sugar receptors and the feeding behaviour of the blowfly. Physiol. Entomol. 14, 127–136 (1989)

    Article  CAS  Google Scholar 

  23. Meunier, N., Marion-Poll, F., Rospars, J. P. & Tanimura, T. Peripheral coding of bitter taste in Drosophila. J. Neurobiol. 56, 139–152 (2003)

    Article  Google Scholar 

  24. Hallem, E. A., Ho, M. G. & Carlson, J. R. The molecular basis of odor coding in the Drosophila antenna. Cell 117, 965–979 (2004)

    Article  CAS  Google Scholar 

  25. Pulver, S. R., Pashkovski, S. L., Hornstein, N. J., Garrity, P. A. & Griffith, L. C. Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J. Neurophysiol. 101, 3075–3088 (2009)

    Article  Google Scholar 

  26. Kwon, Y. et al. Drosophila TRPA1 channel is required to avoid the naturally occurring insect repellent citronellal. Curr. Biol. 20, 1672–1678 (2010)

    Article  CAS  Google Scholar 

  27. Benton, R., Vannice, K. S., Gomez-Diaz, C. & Vosshall, L. B. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149–162 (2009)

    Article  CAS  Google Scholar 

  28. Takken, W. & Knols, B. G. Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu. Rev. Entomol. 44, 131–157 (1999)

    Article  CAS  Google Scholar 

  29. Keller, A., Sweeney, S. T., Zars, T., O'Kane, C. J. & Heisenberg, M. Targeted expression of tetanus neurotoxin interferes with behavioral responses to sensory input in Drosophila. J. Neurobiol. 50, 221–233 (2002)

    Article  CAS  Google Scholar 

  30. Larsson, M. C. et al. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43, 703–714 (2004)

    Article  CAS  Google Scholar 

  31. Kwon, J. Y., Dahanukar, A., Weiss, L. A. & Carlson, J. R. The molecular basis of CO2 reception in Drosophila. Proc. Natl Acad. Sci. USA 104, 3574–3578 (2007)

    Article  ADS  CAS  Google Scholar 

  32. Jones, W. D., Cayirlioglu, P., Kadow, I. G. & Vosshall, L. B. Two chemosensory receptors together mediate carbon dioxide detection in Drosophila. Nature 445, 86–90 (2007)

    Article  ADS  CAS  Google Scholar 

  33. Gaffin, D. D. Electrophysiological analysis of synaptic interactions within peg sensilla of scorpion pectines. Microsc. Res. Tech. 58, 325–334 (2002)

    Article  Google Scholar 

  34. Kazama, H. & Wilson, R. I. Origins of correlated activity in an olfactory circuit. Nature Neurosci. 12, 1136–1144 (2009)

    Article  CAS  Google Scholar 

  35. Yaksi, E. & Wilson, R. I. Electrical coupling between olfactory glomeruli. Neuron 67, 1034–1047 (2010)

    Article  CAS  Google Scholar 

  36. Jones, P. L., Pask, G. M., Rinker, D. C. & Zwiebel, L. J. Functional agonism of insect odorant receptor ion channels. Proc. Natl Acad. Sci. USA 108, 8821–8825 (2011)

    Article  ADS  CAS  Google Scholar 

  37. Suh, G. S. et al. Light activation of an innate olfactory avoidance response in Drosophila. Curr. Biol. 17, 905–908 (2007)

    Article  CAS  Google Scholar 

  38. Ai, M. et al. Acid sensing by the Drosophila olfactory system. Nature 468, 691–695 (2010)

    Article  ADS  CAS  Google Scholar 

  39. Su, C. Y., Martelli, C., Emonet, T. & Carlson, J. R. Temporal coding of odor mixtures in an olfactory receptor neuron. Proc. Natl Acad. Sci. USA 108, 5075–5080 (2011)

    Article  ADS  CAS  Google Scholar 

  40. Martin, J. P. et al. The neurobiology of insect olfaction: sensory processing in a comparative context. Prog. Neurobiol. 95, 427–447 (2011)

    Article  Google Scholar 

  41. van der Goes van Naters, W. & Carlson, J. R. Receptors and neurons for fly odors in Drosophila. Curr. Biol. 17, 606–612 (2007)

    Article  CAS  Google Scholar 

  42. Kurtovic, A., Widmer, A. & Dickson, B. J. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446, 542–546 (2007)

    Article  ADS  CAS  Google Scholar 

  43. Jefferys, J. G. Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol. Rev. 75, 689–723 (1995)

    Article  CAS  Google Scholar 

  44. Faber, D. S. & Korn, H. Electrical field effects: their relevance in central neural networks. Physiol. Rev. 69, 821–863 (1989)

    Article  CAS  Google Scholar 

  45. Kaissling, K. E. Chemo-electrical transduction in insect olfactory receptors. Annu. Rev. Neurosci. 9, 121–145 (1986)

    Article  CAS  Google Scholar 

  46. Nagel, K. I. & Wilson, R. I. Biophysical mechanisms underlying olfactory receptor neuron dynamics. Nature Neurosci. 14, 208–216 (2011)

    Article  CAS  Google Scholar 

  47. Pellegrino, M., Nakagawa, T. & Vosshall, L. B. Single sensillum recordings in the insects Drosophila melanogaster and Anopheles gambiae. J. Vis. Exp. 36, 1–5 (2010)

    Google Scholar 

  48. Cardin, J. A. et al. Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nature Protocols 5, 247–254 (2010)

    Article  CAS  Google Scholar 

  49. Yoo, S. J. et al. Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nature Cell Biol. 4, 416–424 (2002)

    Article  CAS  Google Scholar 

  50. Yao, C. A. & Carlson, J. R. Role of G-proteins in odor-sensing and CO2-sensing neurons in Drosophila. J. Neurosci. 30, 4562–4572 (2010)

    Article  CAS  Google Scholar 

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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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