Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis

Abstract

Chemotaxis in Caenorhabditis elegans, like chemotaxis in bacteria1, involves a random walk biased by the time derivative of attractant concentration2,3, but how the derivative is computed is unknown. Laser ablations have shown that the strongest deficits in chemotaxis to salts are obtained when the ASE chemosensory neurons (ASEL and ASER) are ablated, indicating that this pair has a dominant role4. Although these neurons are left–right homologues anatomically, they exhibit marked asymmetries in gene expression and ion preference5,6,7. Here, using optical recordings of calcium concentration in ASE neurons in intact animals, we demonstrate an additional asymmetry: ASEL is an ON-cell, stimulated by increases in NaCl concentration, whereas ASER is an OFF-cell, stimulated by decreases in NaCl concentration. Both responses are reliable yet transient, indicating that ASE neurons report changes in concentration rather than absolute levels. Recordings from synaptic and sensory transduction mutants show that the ON–OFF asymmetry is the result of intrinsic differences between ASE neurons. Unilateral activation experiments indicate that the asymmetry extends to the level of behavioural output: ASEL lengthens bouts of forward locomotion (runs) whereas ASER promotes direction changes (turns). Notably, the input and output asymmetries of ASE neurons are precisely those of a simple yet novel neuronal motif for computing the time derivative of chemosensory information, which is the fundamental computation of C. elegans chemotaxis3,8. Evidence for ON and OFF cells in other chemosensory networks9,10,11,12 suggests that this motif may be common in animals that navigate by taste and smell.

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: Response of ASEL and ASER to NaCl concentration steps.
Figure 2: Effects of synaptic and signal transduction mutants on ASE sensory responses.
Figure 3: Unilateral activation of ASEL and ASER.
Figure 4: Roles of ASEL and ASER in NaCl step-response behaviour.

References

  1. 1

    Segall, J. E., Block, S. M. & Berg, H. C. Temporal comparisons in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 83, 8987–8991 (1986)

    CAS  Article  ADS  Google Scholar 

  2. 2

    Dusenbery, D. B. Responses of the nematode Caenorhabditis elegans to controlled chemical stimulation. J. Comp. Physiol. 136, 127–331 (1980)

    Google Scholar 

  3. 3

    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 

  4. 4

    Bargmann, C. I. & Horvitz, H. R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans . Neuron 7, 729–742 (1991)

    CAS  Article  Google Scholar 

  5. 5

    Yu, S., Avery, L., Baude, E. & Garbers, D. L. Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc. Natl Acad. Sci. USA 94, 3384–3387 (1997)

    CAS  Article  ADS  Google Scholar 

  6. 6

    Pierce-Shimomura, J. T., Faumont, S., Gaston, M. R., Pearson, B. J. & Lockery, S. R. The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans . Nature 410, 694–698 (2001)

    CAS  Article  ADS  Google Scholar 

  7. 7

    Johnston, R. J., Chang, S., Etchberger, J. F., Ortiz, C. O. & Hobert, O. MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision. Proc. Natl Acad. Sci. USA 102, 12449–12454 (2005)

    CAS  Article  ADS  Google Scholar 

  8. 8

    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 

  9. 9

    Takagi, S. F. & Shibuya, T. ‘On’- and ‘Off’-responses of the olfactory epithelium. Nature 184, 60 (1959)

    CAS  Article  ADS  Google Scholar 

  10. 10

    Mair, R. G. Response properties of rat olfactory bulb neurones. J. Physiol. (Lond.) 326, 341–359 (1982)

    CAS  Article  Google Scholar 

  11. 11

    Hinterwirth, A., Zeiner, R. & Tichy, H. Olfactory receptor cells on the cockroach antennae: responses to the direction and rate of change in food odour concentration. Eur. J. Neurosci. 19, 3389–3392 (2004)

    Article  Google Scholar 

  12. 12

    Liu, L. et al. Drosophila hygrosensation requires the TRP channels water witch and nanchung. Nature 450, 294–298 (2007)

    CAS  Article  ADS  Google Scholar 

  13. 13

    Miyawaki, A. et al. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388, 882–887 (1997)

    CAS  Article  ADS  Google Scholar 

  14. 14

    Schiller, P. H. The ON and OFF channels of the visual system. Trends Neurosci. 15, 86–92 (1992)

    CAS  Article  Google Scholar 

  15. 15

    Richmond, J. E., Davis, W. S. & Jorgensen, E. M. UNC-13 is required for synaptic vesicle fusion in C. elegans . Nature Neurosci. 2, 959–964 (1999)

    CAS  Article  Google Scholar 

  16. 16

    Nonet, M. L., Saifee, O., Zhao, H., Rand, J. B. & Wei, L. Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J. Neurosci. 18, 70–80 (1998)

    CAS  Article  Google Scholar 

  17. 17

    Speese, S. et al. UNC-31 (CAPS) is required for dense-core vesicle but not synaptic vesicle exocytosis in Caenorhabditis elegans . J. Neurosci. 27, 6150–6162 (2007)

    CAS  Article  Google Scholar 

  18. 18

    Coburn, C. M. & Bargmann, C. I. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans . Neuron 17, 695–706 (1996)

    CAS  Article  Google Scholar 

  19. 19

    Komatsu, J., Mori, I., Rhee, J.-S., Akaike, N. & Ohshima, Y. Mutations in a cyclic neucleotide-gated channel lead to abnormal thermosensation and chemosesnation in C. elegans . Neuron 17, 707–718 (1996)

    CAS  Article  Google Scholar 

  20. 20

    Daniels, S. A., Ailion, M., Thomas, J. H. & Sengupta, P. egl-4 acts through a transforming growth factor-beta/SMAD pathway in Caenorhabditis elegans to regulate multiple neuronal circuits in response to sensory cues. Genetics 156, 123–141 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21

    Hirose, T. et al. Cyclic GMP-dependent protein kinase EGL-4 controls body size and lifespan in C. elegans . Development 130, 1089–1099 (2003)

    CAS  Article  Google Scholar 

  22. 22

    L’Etoile, N. D. et al. The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans . Neuron 36, 1079–1089 (2002)

    Article  Google Scholar 

  23. 23

    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 

  24. 24

    Chalasani, S. H. et al. Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans . Nature 450, 63–70 (2007)

    CAS  Article  ADS  Google Scholar 

  25. 25

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

    CAS  Article  Google Scholar 

  26. 26

    Michel, W. C., McClintock, T. S. & Ache, B. W. Inhibition of lobster olfactory receptor cells by an odor-activated potassium conductance. J. Neurophysiol. 65, 446–453 (1991)

    CAS  Article  Google Scholar 

  27. 27

    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 

  28. 28

    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)

    CAS  Article  ADS  Google Scholar 

  29. 29

    Faumont, S., Miller, A. C. & Lockery, S. R. Chemosensory behavior of semi-restrained Caenorhabditis elegans . J. Neurobiol. 65, 171–178 (2005)

    Article  Google Scholar 

  30. 30

    Bargmann, C. I. & Avery, L. Laser killing of cells in Caenorhabditis elegans . Methods Cell Biol. 48, 225–250 (1995)

    CAS  Article  Google Scholar 

  31. 31

    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 

  32. 32

    Winer, B. J., Brown, D. R. & Michels, K. M. Statistica Principles in Experimental Design 3rd ed. 354–358 (McGraw-Hill, Boston, 1991)

    Google Scholar 

Download references

Acknowledgements

We thank the Caenorhabditis Genetics Center for strains, C. Frøkjœr-Jensen for strain integration and D. Julius for the TRPV1 complementary DNA. Support was provided by grants from the National Institutes of Health (MH051383 to S.R.L.; DA016445 to W.R.S.), National Science Foundation (IOB-0543643 to S.R.L.) and Human Frontier Science Program (to W.R.S.).

Author Contributions H.S. planned and performed the experiments first revealing the ASE ON–OFF function and the effects of transduction and synaptic mutants, made imaging and direct activation reagents, acquired supplementary ion-sensitivity data and drafted the manuscript. T.R.T. planned and performed ON–OFF, dose-response, genetics, direct activation and ablation experiments in the text and Supplementary Information, made imaging reagents, generated figures, and co-wrote the final manuscript. S.F. planned and performed ion selectivity and synaptic mutant imaging in the text and Supplementary Information. M.E. developed dose-response methodologies. S.R.L. planned imaging and behavioural experiments, devised the derivative model, and co-wrote the final manuscript. W.R.S. planned imaging and genetics experiments, and drafted the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Shawn R. Lockery.

Supplementary information

Supplementary information

The file contains Supplementary Notes with experimental procedures and Supplementary Figures 1-6 with Legends (PDF 4807 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Suzuki, H., Thiele, T., Faumont, S. et al. Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature 454, 114–117 (2008). https://doi.org/10.1038/nature06927

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