Skip to main content
SpringerLink
Log in

Methods to Study Nervous System Laterality in the Caenorhabditis elegans Model System

  • Protocol
  • First Online:
Lateralized Brain Functions

Part of the book series: Neuromethods ((NM,volume 122))

Abstract

The anatomically and genetically very accessible nervous system of the nematode Caenorhabditis elegans, composed of a total of 302 neurons in the hermaphrodite, displays a number of striking neuronal lateralities which come largely in two forms: unilateral neurons found only on one side of the nervous system and functional differences in otherwise bilaterally symmetric neuron pairs. Two recent reviews have described in detail the genetic mechanisms that specify the most prominent sensory lateralities in two bilaterally symmetric sensory neuron classes in C. elegans. In this Neuromethods chapter, we provide a general overview of the specific methods and opportunities that exist in C. elegans to identify lateralities, to decipher their functional relevance and to dissect the genetic control mechanisms that establish these lateralities. These specific advantages include (a) the ability to identify and visualize neuronal lateralities on the anatomical, gene expression, and neuronal activity level with single cell resolution; (b) the ability to assign function to lateralized neurons using behavioral analysis and genetic manipulation of neuronal activity; (c) the ability to conduct genetic screens for mutants that disrupt lateralities, thereby deciphering the genetic patterning mechanisms that instruct neuronal lateralities.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Rogers LJ, Vallortigara G, Andrew RJ (2013) Divided brains: the biology and behavior of brain asymmetries. Cambridge University Press, Cambridge

    Book  Google Scholar 

  2. Davidson RJ, Hugdahl K (eds) (1994) Brain asymmetry. MIT Press, Cambridge, MA

    Google Scholar 

  3. Hugdahl K, Davidson RJ (eds) (2003) The asymmetrical brain. MIT Press, Cambridge, MA

    Google Scholar 

  4. Concha ML, Bianco IH, Wilson SW (2012) Encoding asymmetry within neural circuits. Nat Rev Neurosci 13:832–843

    Article  CAS  PubMed  Google Scholar 

  5. Sun T, Walsh CA (2006) Molecular approaches to brain asymmetry and handedness. Nat Rev Neurosci 7:655–662

    Article  CAS  PubMed  Google Scholar 

  6. Hobert O, Johnston RJ Jr, Chang S (2002) Left-right asymmetry in the nervous system: the Caenorhabditis elegans model. Nat Rev Neurosci 3:629–640

    Article  CAS  PubMed  Google Scholar 

  7. Frasnelli E, Vallortigara G, Rogers LJ (2012) Left-right asymmetries of behaviour and nervous system in invertebrates. Neurosci Biobehav Rev 36:1273–1291

    Article  PubMed  Google Scholar 

  8. White JG, Southgate E, Thomson JN, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 314:1–340

    Article  CAS  PubMed  Google Scholar 

  9. Hobert O (2014) Development of left/right asymmetry in the Caenorhabditis elegans nervous system: from zygote to postmitotic neuron. Genesis 52:528–543

    Article  PubMed  Google Scholar 

  10. Hsieh YW, Alqadah A, Chuang CF (2014) Asymmetric neural development in the Caenorhabditis elegans olfactory system. Genesis 52:544–554

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hall DH, Altun Z (2007) C. elegans atlas. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  12. McIntire SL, Jorgensen E, Kaplan J, Horvitz HR (1993) The GABAergic nervous system of Caenorhabditis elegans. Nature 364:337–341

    Article  CAS  PubMed  Google Scholar 

  13. Turek M, Lewandrowski I, Bringmann H (2013) An AP2 transcription factor is required for a sleep-active neuron to induce sleep-like quiescence in C. elegans. Curr Biol 23:2215–2223

    Article  CAS  PubMed  Google Scholar 

  14. Van Buskirk C, Sternberg PW (2007) Epidermal growth factor signaling induces behavioral quiescence in Caenorhabditis elegans. Nat Neurosci 10:1300–1307

    Article  PubMed  Google Scholar 

  15. Sulston JE, Horvitz HR (1977) Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56:110–156

    Article  CAS  PubMed  Google Scholar 

  16. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64–119

    Article  CAS  PubMed  Google Scholar 

  17. Greenwald IS, Sternberg PW, Horvitz HR (1983) The lin-12 locus specifies cell fates in Caenorhabditis elegans. Cell 34:435–444

    Article  CAS  PubMed  Google Scholar 

  18. Lambie EJ, Kimble J (1991) Two homologous regulatory genes, lin-12 and glp-1, have overlapping functions. Development 112:231–240

    CAS  PubMed  Google Scholar 

  19. Hutter H, Schnabel R (1995) Establishment of left-right asymmetry in the Caenorhabditis elegans embryo: a multistep process involving a series of inductive events. Development 121:3417–3424

    CAS  PubMed  Google Scholar 

  20. Moskowitz IP, Rothman JH (1996) lin-12 and glp-1 are required zygotically for early embryonic cellular interactions and are regulated by maternal GLP-1 signaling in Caenorhabditis elegans. Development 122:4105–4117

    CAS  PubMed  Google Scholar 

  21. Priess JR (2005) Notch signaling in the C. elegans embryo. In: WormBook, C.e.R. Community (ed). WormBook. doi:10.1895/wormbook.1.4.1, http://www.wormbook.org

  22. Hermann GJ, Leung B, Priess JR (2000) Left-right asymmetry in C. elegans intestine organogenesis involves a LIN-12/Notch signaling pathway. Development 127:3429–3440

    CAS  PubMed  Google Scholar 

  23. Lin R, Hill RJ, Priess JR (1998) POP-1 and anterior-posterior fate decisions in C. elegans embryos. Cell 92:229–239

    Article  CAS  PubMed  Google Scholar 

  24. Hutter H, Schnabel R (1994) glp-1 and inductions establishing embryonic axes in C. elegans. Development 120:2051–2064

    CAS  PubMed  Google Scholar 

  25. Cochella L, Hobert O (2012) Embryonic priming of a miRNA locus predetermines postmitotic neuronal left/right asymmetry in C. elegans. Cell 151:1229–1242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263:802–805

    Article  CAS  PubMed  Google Scholar 

  27. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83:207–218

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Troemel ER, Sagasti A, Bargmann CI (1999) Lateral signaling mediated by axon contact and calcium entry regulates asymmetric odorant receptor expression in C. elegans. Cell 99:387–398

    Article  CAS  PubMed  Google Scholar 

  30. Lesch BJ, Bargmann CI (2010) The homeodomain protein hmbx-1 maintains asymmetric gene expression in adult C. elegans olfactory neurons. Genes Dev 24:1802–1815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ortiz CO, Etchberger JF, Posy SL, Frokjaer-Jensen C, Lockery S, Honig B, Hobert O (2006) Searching for neuronal left/right asymmetry: genomewide analysis of nematode receptor-type guanylyl cyclases. Genetics 173:131–149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Johnston RJ Jr, Chang S, Etchberger JF, Ortiz CO, Hobert O (2005) MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision. Proc Natl Acad Sci U S A 102:12449–12454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77:71–94

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Doitsidou M, Poole RJ, Sarin S, Bigelow H, Hobert O (2010) C. elegans mutant identification with a one-step whole-genome-sequencing and SNP mapping strategy. PLoS ONE 5:e15435

    Article  PubMed  PubMed Central  Google Scholar 

  35. Hobert O, Tessmar K, Ruvkun G (1999) The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons. Development 126:1547–1562

    CAS  PubMed  Google Scholar 

  36. Johnston RJ, Hobert O (2003) A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426:845–849

    Article  CAS  PubMed  Google Scholar 

  37. Sarin S, Prabhu S, O'Meara MM, Pe'er I, Hobert O (2008) Caenorhabditis elegans mutant allele identification by whole-genome sequencing. Nat Methods 5:865–867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Zhang F, O'Meara MM, Hobert O (2011) A left/right asymmetric neuronal differentiation program is controlled by the Caenorhabditis elegans lsy-27 zinc-finger transcription factor. Genetics 188:753–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Flowers EB, Poole RJ, Tursun B, Bashllari E, Pe'er I, Hobert O (2010) The Groucho ortholog UNC-37interacts with the short Groucho-like protein LSY-22 to control developmental decisions in C. elegans. Development 137:1799–1805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Sarin S, Bertrand V, Bigelow H, Boyanov A, Doitsidou M, Poole RJ, Narula S, Hobert O (2010) Analysis of multiple ethyl methanesulfonate-mutagenized caenorhabditis elegans strains by whole-genome sequencing. Genetics 185:417–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Dusenbery DB (1974) Analysis of chemotaxis in the nematode Caenorhabditis elegans by countercurrent separation. J Exp Zool 188:41–47

    Article  CAS  PubMed  Google Scholar 

  42. Ward S (1973) Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by use of mutants. Proc Natl Acad Sci U S A 70:817–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Hedgecock EM, Russell RL (1975) Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 72:4061–4065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Bargmann CI, Hartwieg E, Horvitz HR (1993) Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74:515–527

    Article  CAS  PubMed  Google Scholar 

  45. Bargmann CI, Horvitz HR (1991) Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7:729–742

    Article  CAS  PubMed  Google Scholar 

  46. Pierce-Shimomura JT, Faumont S, Gaston MR, Pearson BJ, Lockery SR (2001) The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans. Nature 410:694–698

    Article  CAS  PubMed  Google Scholar 

  47. Wes PD, Bargmann CI (2001) C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature 410:698–701

    Article  CAS  PubMed  Google Scholar 

  48. Ortiz CO, Faumont S, Takayama J, Ahmed HK, Goldsmith AD, Pocock R, McCormick KE, Kunimoto H, Iino Y, Lockery S et al (2009) Lateralized gustatory behavior of C. elegans is controlled by specific receptor-type guanylyl cyclases. Curr Biol 19:996–1004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Glock C, Nagpal J, Gottschalk A (2015) Microbial rhodopsin optogenetic tools: application for analyses of synaptic transmission and of neuronal network activity in behavior. Methods Mol Biol 1327:87–103

    Article  CAS  PubMed  Google Scholar 

  50. Toga AW, Thompson PM (2003) Mapping brain asymmetry. Nat Rev Neurosci 4:37–48

    Article  CAS  PubMed  Google Scholar 

  51. Suzuki H, Thiele TR, Faumont S, Ezcurra M, Lockery SR, Schafer WR (2008) Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature 454:114–117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Bertrand V, Bisso P, Poole RJ, Hobert O (2011) Notch-dependent induction of left/right asymmetry in C. elegans interneurons and motoneurons. Curr Biol 21:1225–1231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Prevedel R, Yoon YG, Hoffmann M, Pak N, Wetzstein G, Kato S, Schrodel T, Raskar R, Zimmer M, Boyden ES et al (2014) Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy. Nat Methods 11:727–730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Boulin T, Etchberger JF, Hobert O (2006). Reporter gene fusions. WormBook, pp 1–23

    Google Scholar 

  55. Minevich G, Park DS, Blankenberg D, Poole RJ, Hobert O (2012) CloudMap: a cloud-based pipeline for analysis of mutant genome sequences. Genetics 192:1249–1269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Left/right asymmetry research in the Hobert laboratory has been funded by the National Institutes of Health and the Howard Hughes Medical Institute.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, NY, USA

    Berta Vidal

  2. Department of Biochemistry and Molecular Biophysics, Columbia University, Howard Hughes Medical Institute, New York, NY, USA

    Oliver Hobert

Authors
  1. Berta Vidal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Oliver Hobert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Berta Vidal .

Editor information

Editors and Affiliations

  1. School of Science and Technology, University of New England, Armidale, Australia

    Lesley J. Rogers

  2. Centre for Mind/Brain Sciences, University of Trento, Trento, Trento, Italy

    Giorgio Vallortigara

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer Science+Business Media LLC

About this protocol

Cite this protocol

Vidal, B., Hobert, O. (2017). Methods to Study Nervous System Laterality in the Caenorhabditis elegans Model System. In: Rogers, L., Vallortigara, G. (eds) Lateralized Brain Functions. Neuromethods, vol 122. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6725-4_18

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-6725-4_18

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-6723-0

  • Online ISBN: 978-1-4939-6725-4

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation