Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans

A Corrigendum to this article was published on 20 January 2016

A Corrigendum to this article was published on 03 January 2008

Abstract

Although many properties of the nervous system are shared among animals and systems, it is not known whether different neuronal circuits use common strategies to guide behaviour. Here we characterize information processing by Caenorhabditis elegans olfactory neurons (AWC) and interneurons (AIB and AIY) that control food- and odour-evoked behaviours. Using calcium imaging and mutations that affect specific neuronal connections, we show that AWC neurons are activated by odour removal and activate the AIB interneurons through AMPA-type glutamate receptors. The level of calcium in AIB interneurons is elevated for several minutes after odour removal, a neuronal correlate to the prolonged behavioural response to odour withdrawal. The AWC neuron inhibits AIY interneurons through glutamate-gated chloride channels; odour presentation relieves this inhibition and results in activation of AIY interneurons. The opposite regulation of AIY and AIB interneurons generates a coordinated behavioural response. Information processing by this circuit resembles information flow from vertebrate photoreceptors to ‘OFF’ bipolar and ‘ON’ bipolar neurons, indicating a conserved or convergent strategy for sensory information processing.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: AWC responds to odour removal.
Figure 2: Both classes of AWC neurons respond to odour removal.
Figure 3: Calcium responses in AIB and AIY interneurons.
Figure 4: AWC neurons signal through glutamate and glutamate receptors.
Figure 5: AIB and AIY require different glutamate receptors.
Figure 6: Odour-regulated turning behaviours.

References

  1. 1

    Milo, R. et al. Network motifs: simple building blocks of complex networks. Science 298, 824–827 (2002)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Chalfie, M. et al. The neural circuit for touch sensitivity in Caenorhabditis elegans . J. Neurosci. 5, 956–964 (1985)

    CAS  Article  Google Scholar 

  3. 3

    White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. The structure of the nervous system of the nematode Caenorhabditis elegans . Phil. Trans. R. Soc. Lond. B 314, 1–340 (1986)

    ADS  CAS  Article  Google Scholar 

  4. 4

    de Bono, M. & Maricq, A. V. Neuronal substrates of complex behaviors in C. elegans . Annu. Rev. Neurosci. 28, 451–501 (2005)

    CAS  Article  Google Scholar 

  5. 5

    Bargmann, C. I. in Wormbook (ed. The C. elegans Research Community) WormBook doi/10.1895/wormbook.1.123. 1 〈http://www.wormbook.org〉 (2006)

    Google Scholar 

  6. 6

    Zheng, Y., Brockie, P. J., Mellem, J. E., Madsen, D. M. & Maricq, A. V. Neuronal control of locomotion in C. elegans is modified by a dominant mutation in the GLR-1 ionotropic glutamate receptor. Neuron 24, 347–361 (1999)

    CAS  Article  Google Scholar 

  7. 7

    Tobin, D. et al. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35, 307–318 (2002)

    CAS  Article  Google Scholar 

  8. 8

    Goodman, M. B., Hall, D. H., Avery, L. & Lockery, S. R. Active currents regulate sensitivity and dynamic range in C. elegans neurons. Neuron 20, 763–772 (1998)

    CAS  Article  Google Scholar 

  9. 9

    Kerr, R. et al. Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans . Neuron 26, 583–594 (2000)

    CAS  Article  Google Scholar 

  10. 10

    Mellem, J. E., Brockie, P. J., Zheng, Y., Madsen, D. M. & Maricq, A. V. Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. elegans . Neuron 36, 933–944 (2002)

    CAS  Article  Google Scholar 

  11. 11

    Pierce-Shimomura, J. T., Morse, T. M. & Lockery, S. R. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J. Neurosci. 19, 9557–9569 (1999)

    CAS  Article  Google Scholar 

  12. 12

    Hills, T., Brockie, P. J. & Maricq, A. V. Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans . J. Neurosci. 24, 1217–1225 (2004)

    CAS  Article  Google Scholar 

  13. 13

    Wakabayashi, T., Kitagawa, I. & Shingai, R. Neurons regulating the duration of forward locomotion in Caenorhabditis elegans . Neurosci. Res. 50, 103–111 (2004)

    Article  Google Scholar 

  14. 14

    Gray, J. M., Hill, J. J. & Bargmann, C. I. A circuit for navigation in Caenorhabditis elegans . Proc. Natl Acad. Sci. USA 102, 3184–3191 (2005)

    ADS  CAS  Article  Google Scholar 

  15. 15

    Zhao, B., Khare, P., Feldman, L. & Dent, J. A. Reversal frequency in Caenorhabditis elegans represents an integrated response to the state of the animal and its environment. J. Neurosci. 23, 5319–5328 (2003)

    CAS  Article  Google Scholar 

  16. 16

    Nakai, J., Ohkura, M. & Imoto, K. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nature Biotechnol. 19, 137–141 (2001)

    CAS  Article  Google Scholar 

  17. 17

    Pologruto, T. A., Yasuda, R. & Svoboda, K. Monitoring neural activity and [Ca2+] with genetically encoded Ca2+ indicators. J. Neurosci. 24, 9572–9579 (2004)

    CAS  Article  Google Scholar 

  18. 18

    Jospin, M., Jacquemond, V., Mariol, M. C., Segalat, L. & Allard, B. The L-type voltage-dependent Ca2+ channel EGL-19 controls body wall muscle function in Caenorhabditis elegans . J. Cell Biol. 159, 337–348 (2002)

    CAS  Article  Google Scholar 

  19. 19

    Chronis, N., Zimmer, M. & Bargmann, C. I. Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans . Nature Methods 4, 727–731 (2007)

    CAS  Article  Google Scholar 

  20. 20

    Bargmann, C. I., Hartwieg, E. & Horvitz, H. R. Odorant-selective genes and neurons mediate olfaction in C. elegans . Cell 74, 515–527 (1993)

    CAS  Article  Google Scholar 

  21. 21

    Colbert, H. A. & Bargmann, C. I. Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans . Learn. Mem. 4, 179–191 (1997)

    CAS  Article  Google Scholar 

  22. 22

    Wes, P. D. & Bargmann, C. I. C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature 410, 698–701 (2001)

    ADS  CAS  Article  Google Scholar 

  23. 23

    Major, G. & Tank, D. Persistent neural activity: prevalence and mechanisms. Curr. Opin. Neurobiol. 14, 675–684 (2004)

    CAS  Article  Google Scholar 

  24. 24

    Davis, R. E. & Stretton, A. O. W. Signalling properties of Ascaris motor neurons: graded synaptic transmission and tonic transmitter release. J. Neurosci. 9, 415–425 (1989)

    CAS  Article  Google Scholar 

  25. 25

    Clark, D. A., Biron, D., Sengupta, P. & Samuel, A. D. The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans . J. Neurosci. 26, 7444–7451 (2006)

    CAS  Article  Google Scholar 

  26. 26

    Lee, R. Y., Sawin, E. R., Chalfie, M., Horvitz, H. R. & Avery, L. EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in Caenorhabditis elegans . J. Neurosci. 19, 159–167 (1999)

    CAS  Article  Google Scholar 

  27. 27

    Hart, A. C., Sims, S. & Kaplan, J. M. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378, 82–85 (1995)

    ADS  CAS  Article  Google Scholar 

  28. 28

    Maricq, A. V., Peckol, E., Driscoll, M. & Bargmann, C. I. Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378, 78–81 (1995)

    ADS  CAS  Article  Google Scholar 

  29. 29

    Cully, D. F. et al. Cloning of an avermectin-sensitive glutamate-gated chloride channel from Caenorhabditis elegans . Nature 371, 707–711 (1994)

    ADS  CAS  Article  Google Scholar 

  30. 30

    Dillon, J., Hopper, N. A., Holden-Dye, L. & O’Connor, V. Molecular characterization of the metabotropic glutamate receptor family in Caenorhabditis elegans . Biochem. Soc. Trans. 34, 942–948 (2006)

    CAS  Article  Google Scholar 

  31. 31

    Chou, J. H., Bargmann, C. I. & Sengupta, P. The Caenorhabditis elegans odr-2 gene encodes a novel Ly-6-related protein required for olfaction. Genetics 157, 211–224 (2001)

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32

    Horoszok, L., Raymond, V., Sattelle, D. B. & Wolstenholme, A. J. GLC-3: a novel fipronil and BIDN-sensitive, but picrotoxin-insensitive, l-glutamate-gated chloride channel subunit from Caenorhabditis elegans . Br. J. Pharmacol. 132, 1247–1254 (2001)

    CAS  Article  Google Scholar 

  33. 33

    Wenick, A. S. & Hobert, O. Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans . Dev. Cell 6, 757–770 (2004)

    CAS  Article  Google Scholar 

  34. 34

    Malinow, R. & Malenka, R. C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103–126 (2002)

    CAS  Article  Google Scholar 

  35. 35

    Miller, A. C., Thiele, T. R., Faumont, S., Moravec, M. L. & Lockery, S. R. Step-response analysis of chemotaxis in Caenorhabditis elegans . J. Neurosci. 25, 3369–3378 (2005)

    CAS  Article  Google Scholar 

  36. 36

    Brockie, P. J., Madsen, D. M., Zheng, Y., Mellem, J. & Maricq, A. V. Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. J. Neurosci. 21, 1510–1522 (2001)

    CAS  Article  Google Scholar 

  37. 37

    Zhang, X. & Cote, R. H. cGMP signaling in vertebrate retinal photoreceptor cells. Front. Biosci. 10, 1191–1204 (2005)

    CAS  Article  Google Scholar 

  38. 38

    Furukawa, T., Morrow, E. M. & Cepko, C. L. Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91, 531–541 (1997)

    CAS  Article  Google Scholar 

  39. 39

    Lanjuin, A., VanHoven, M. K., Bargmann, C. I., Thompson, J. K. & Sengupta, P. Otx/otd homeobox genes specify distinct sensory neuron identities in C. elegans . Dev. Cell 5, 621–633 (2003)

    CAS  Article  Google Scholar 

  40. 40

    Yang, X.-L. Characterization of receptors for glutamate and GABA in retinal neurons. Prog. Neurobiol. 73, 127–150 (2004)

    CAS  Article  Google Scholar 

  41. 41

    Wassle, H. Parallel processing in the mammalian retina. Nature Rev. Neurosci. 5, 747–757 (2004)

    Article  Google Scholar 

  42. 42

    Grant, G. B. & Dowling, J. E. A glutamate-activated chloride current in cone-driven ON bipolar cells of the white Perch retina. J. Neurosci. 15, 3852–3862 (1995)

    CAS  Article  Google Scholar 

  43. 43

    Schiller, P. H., Sandell, J. H. & Maunsell, J. H. Functions of the ON and OFF channels of the visual system. Nature 322, 824–825 (1986)

    ADS  CAS  Article  Google Scholar 

  44. 44

    Taha, S. A. & Fields, H. L. Inhibitions of nucleus accumbens neurons encode a gating signal for reward-directed behavior. J. Neurosci. 26, 217–222 (2006)

    CAS  Article  Google Scholar 

  45. 45

    Berg, H. C. & Brown, D. A. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239, 500–504 (1972)

    ADS  CAS  Article  Google Scholar 

  46. 46

    Dusenbery, D. B. Responses of the nematode Caenorhabditis elegans to controlled chemical stimulation. J. Comp. Physiol. 136, 327–331 (1980)

    Article  Google Scholar 

  47. 47

    Ryu, W. S. & Samuel, A. D. Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined thermal stimuli. J. Neurosci. 22, 5727–5733 (2002)

    CAS  Article  Google Scholar 

  48. 48

    Zariwala, H. A., Miller, A. C., Faumont, S. & Lockery, S. R. Step response analysis of thermotaxis in Caenorhabditis elegans . J. Neurosci. 23, 4369–4377 (2003)

    CAS  Article  Google Scholar 

  49. 49

    Mori, I. & Ohshima, Y. Neural regulation of thermotaxis in Caenorhabditis elegans . Nature 376, 344–348 (1995)

    ADS  CAS  Article  Google Scholar 

  50. 50

    Zhang, Y., Lu, H. & Bargmann, C. I. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans . Nature 438, 179–184 (2005)

    ADS  CAS  Article  Google Scholar 

  51. 51

    Younan, X. & Whitesides, G. Soft lithography. Ann. Rev. Mater. Sci. 28, 153–184 (1998)

    ADS  Article  Google Scholar 

Download references

Acknowledgements

We thank the C. elegans Knockout Consortium and the Caenorhabditis Genetic Center (CGC) for strains, A. Wolstenholme for the glc-3 cDNA, P. Sengupta for the srsx-3 promoter, and M. Meister, M. Zimmer, B. Snyder, G. Lee, D. Albrecht, M. Hilliard and other Bargmann laboratory members for critical help, insights and advice. S.H.C. was supported by the Damon Runyon Cancer Research Foundation and C.I.B. is an Investigator of the Howard Hughes Medical Institute. This work was supported by the Howard Hughes Medical Institute (C.I.B.) and the Klingenstein Fund for Neuroscience (M.B.G.).

Author Contributions S.H.C. designed and performed experiments, analysed data and wrote the paper; N.C., M.T. and J.M.G. designed and performed experiments; D.R. and M.B.G. developed analytical tools; and C.I.B. designed experiments, analysed data and wrote the paper.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Cornelia I. Bargmann.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Methods with additional references, Supplementary Figures S1-S8 with Legends, Supplementary Movie Legends and Supplementary Table S1. (PDF 27989 kb)

Supplementary Movie 1

The file contains Supplementary Movie 1 showing calcium responses in AWC after removal of stimulus. (MOV 5858 kb)

Supplementary Movie 2

The file contains Supplementary Movie 2 showing calcium responses in AIB after removal of stimulus. (MOV 4663 kb)

Supplementary Movie 3

The file contains Supplementary Movie 3 showing calcium responses in AIY after addition of stimulus. (MOV 7487 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Chalasani, S., Chronis, N., Tsunozaki, M. et al. Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450, 63–70 (2007). https://doi.org/10.1038/nature06292

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing