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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1993 Mar 15;90(6):2227–2231. doi: 10.1073/pnas.90.6.2227

A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans.

J M Kaplan 1, H R Horvitz 1
PMCID: PMC46059  PMID: 8460126

Abstract

After light touch to its nose, the nematode Caenorhabditis elegans halts forward locomotion and initiates backing. Here we show that three classes of neurons (ASH, FLP, and OLQ) sense touch to the nose and hence are required for this avoidance response. ASH, FLP, and OLQ have sensory endings that contain axonemal cilia. Mutant animals that have defective ciliated sensory endings as well as laser-operated animals that lack ASH, FLP, and OLQ fail to respond to touch to the nose. Together with the previous work of others, these results demonstrate that C. elegans has at least five morphologically distinct classes of mechanosensory neurons. Interestingly, the ASH neuron also acts as a chemosensory neuron; it mediates the avoidance of noxious chemicals. Since ASH possesses both chemosensory and mechanosensory modalities, this neuron might be functionally analogous to vertebrate nociceptors, which mediate the sensation of pain.

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Selected References

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  1. Albert P. S., Brown S. J., Riddle D. L. Sensory control of dauer larva formation in Caenorhabditis elegans. J Comp Neurol. 1981 May 20;198(3):435–451. doi: 10.1002/cne.901980305. [DOI] [PubMed] [Google Scholar]
  2. Albertson D. G., Thomson J. N. The pharynx of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci. 1976 Aug 10;275(938):299–325. doi: 10.1098/rstb.1976.0085. [DOI] [PubMed] [Google Scholar]
  3. Avery L., Horvitz H. R. Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron. 1989 Oct;3(4):473–485. doi: 10.1016/0896-6273(89)90206-7. [DOI] [PubMed] [Google Scholar]
  4. Bargmann C. I., Horvitz H. R. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron. 1991 Nov;7(5):729–742. doi: 10.1016/0896-6273(91)90276-6. [DOI] [PubMed] [Google Scholar]
  5. Bargmann C. I., Horvitz H. R. Control of larval development by chemosensory neurons in Caenorhabditis elegans. Science. 1991 Mar 8;251(4998):1243–1246. doi: 10.1126/science.2006412. [DOI] [PubMed] [Google Scholar]
  6. Bargmann C. I., Thomas J. H., Horvitz H. R. Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol. 1990;55:529–538. doi: 10.1101/sqb.1990.055.01.051. [DOI] [PubMed] [Google Scholar]
  7. Besson J. M., Chaouch A. Peripheral and spinal mechanisms of nociception. Physiol Rev. 1987 Jan;67(1):67–186. doi: 10.1152/physrev.1987.67.1.67. [DOI] [PubMed] [Google Scholar]
  8. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94. doi: 10.1093/genetics/77.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chalfie M., Au M. Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science. 1989 Feb 24;243(4894 Pt 1):1027–1033. doi: 10.1126/science.2646709. [DOI] [PubMed] [Google Scholar]
  10. Chalfie M., Sulston J. E., White J. G., Southgate E., Thomson J. N., Brenner S. The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci. 1985 Apr;5(4):956–964. doi: 10.1523/JNEUROSCI.05-04-00956.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chalfie M., Sulston J. Developmental genetics of the mechanosensory neurons of Caenorhabditis elegans. Dev Biol. 1981 Mar;82(2):358–370. doi: 10.1016/0012-1606(81)90459-0. [DOI] [PubMed] [Google Scholar]
  12. Chalfie M., Thomson J. N. Organization of neuronal microtubules in the nematode Caenorhabditis elegans. J Cell Biol. 1979 Jul;82(1):278–289. doi: 10.1083/jcb.82.1.278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hamelin M., Scott I. M., Way J. C., Culotti J. G. The mec-7 beta-tubulin gene of Caenorhabditis elegans is expressed primarily in the touch receptor neurons. EMBO J. 1992 Aug;11(8):2885–2893. doi: 10.1002/j.1460-2075.1992.tb05357.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hasan Z., Stuart D. G. Animal solutions to problems of movement control: the role of proprioceptors. Annu Rev Neurosci. 1988;11:199–223. doi: 10.1146/annurev.ne.11.030188.001215. [DOI] [PubMed] [Google Scholar]
  15. Hedgecock E. M., Culotti J. G., Thomson J. N., Perkins L. A. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev Biol. 1985 Sep;111(1):158–170. doi: 10.1016/0012-1606(85)90443-9. [DOI] [PubMed] [Google Scholar]
  16. Heiligenberg W. The neural basis of behavior: a neuroethological view. Annu Rev Neurosci. 1991;14:247–267. doi: 10.1146/annurev.ne.14.030191.001335. [DOI] [PubMed] [Google Scholar]
  17. Herman R. K., Hedgecock E. M. Limitation of the size of the vulval primordium of Caenorhabditis elegans by lin-15 expression in surrounding hypodermis. Nature. 1990 Nov 8;348(6297):169–171. doi: 10.1038/348169a0. [DOI] [PubMed] [Google Scholar]
  18. Horvitz H. R., Brenner S., Hodgkin J., Herman R. K. A uniform genetic nomenclature for the nematode Caenorhabditis elegans. Mol Gen Genet. 1979 Sep;175(2):129–133. doi: 10.1007/BF00425528. [DOI] [PubMed] [Google Scholar]
  19. Lewis J. A., Hodgkin J. A. Specific neuroanatomical changes in chemosensory mutants of the nematode Caenorhabditis elegans. J Comp Neurol. 1977 Apr 1;172(3):489–510. doi: 10.1002/cne.901720306. [DOI] [PubMed] [Google Scholar]
  20. Perkins L. A., Hedgecock E. M., Thomson J. N., Culotti J. G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev Biol. 1986 Oct;117(2):456–487. doi: 10.1016/0012-1606(86)90314-3. [DOI] [PubMed] [Google Scholar]
  21. Sulston J. E., Horvitz H. R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol. 1977 Mar;56(1):110–156. doi: 10.1016/0012-1606(77)90158-0. [DOI] [PubMed] [Google Scholar]
  22. Sulston J. E., Schierenberg E., White J. G., Thomson J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983 Nov;100(1):64–119. doi: 10.1016/0012-1606(83)90201-4. [DOI] [PubMed] [Google Scholar]
  23. Thomas J. H. Genetic analysis of defecation in Caenorhabditis elegans. Genetics. 1990 Apr;124(4):855–872. doi: 10.1093/genetics/124.4.855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ward S., Thomson N., White J. G., Brenner S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans.?2UU. J Comp Neurol. 1975 Apr 1;160(3):313–337. doi: 10.1002/cne.901600305. [DOI] [PubMed] [Google Scholar]
  25. Way J. C., Chalfie M. The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev. 1989 Dec;3(12A):1823–1833. doi: 10.1101/gad.3.12a.1823. [DOI] [PubMed] [Google Scholar]
  26. Woolf C. J., Walters E. T. Common patterns of plasticity contributing to nociceptive sensitization in mammals and Aplysia. Trends Neurosci. 1991 Feb;14(2):74–78. doi: 10.1016/0166-2236(91)90024-o. [DOI] [PubMed] [Google Scholar]

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