Skip to main content
SpringerLink
Log in

Optically Monitoring and Manipulating Brain and Behavior in C. elegans

  • Chapter
  • First Online:
Book cover New Techniques in Systems Neuroscience

Part of the book series: Biological and Medical Physics, Biomedical Engineering ((BIOMEDICAL))

  • 1746 Accesses

Abstract

Small animals such as the nematode C. elegans offer the possibility of understanding how an integrated nervous system in a live animal drives complex behaviors. The last decade has seen rapid progress in fluorescent genetically encoded optical probes of neuronal activity. These now permit physiological analysis of worm neural circuits using light microscopy, ideal for the small, transparent, genetically tractable nematode. C. elegans researchers can now dissect the activity patterns of virtually any cell in live animals. Here, we review progress on microscopy and instrumentation that allow one to use genetically encoded probes to connect brain and behavior in C. elegans.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
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. Abrahamsson, S., Chen, J., Hajj, B., et al. (2012). Fast multicolor 3D imaging using aberration-corrected multifocus microscopy. Nature Methods, 10, 60–63. doi:10.1038/nmeth.2277.

    Article  Google Scholar 

  2. Ahrens, M. B., Orger, M. B., Robson, D. N., et al. (2013). Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nature Methods, 10, 413–420. doi:10.1038/nmeth.2434.

    Article  Google Scholar 

  3. Albrecht, D. R., & Bargmann, C. I. (2011). High-content behavioral analysis of Caenorhabditis elegans in precise spatiotemporal chemical environments. Nature Methods, 8, 599–605. doi:10.1038/nmeth.1630.

    Article  Google Scholar 

  4. Bargmann, C. I., & Horvitz, H. R. (1991). Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron, 7, 729–742. doi:10.1016/0896-6273(91)90276-6.

    Article  Google Scholar 

  5. Biron, D., Shibuya, M., Gabel, C., et al. (2006). A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans. Nature Neuroscience, 9, 1499–1505. doi:10.1038/nn1796.

    Article  Google Scholar 

  6. Boyden, E. S., Zhang, F., Bamberg, E., et al. (2005). Millisecond-timescale, genetically targeted optical control of neural activity. Nature Neuroscience, 8, 1263–1268. doi:10.1038/nn1525.

    Article  Google Scholar 

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

    Article  ADS  Google Scholar 

  8. Chalfie, M., Sulston, J. E., White, J. G., et al. (1985). The neural circuit for touch sensitivity in Caenorhabditis elegans. Journal of Neuroscience, 5, 956–964.

    Google Scholar 

  9. Chow, B. Y., Han, X., Dobry, A. S., et al. (2010). High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature, 463, 98–102. doi:10.1038/nature08652.

    Article  ADS  Google Scholar 

  10. Chronis, N., Zimmer, M., & Bargmann, C. I. (2007). Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nature Methods, 4, 727–731.doi:10.1038/nmeth1075.

    Article  Google Scholar 

  11. Chuong, A. S., Miri, M. L., Busskamp, V., et al. (2014). Noninvasive optical inhibition with a red-shifted microbial rhodopsin. Nature Neuroscience, 17, 1123–1129. doi:10.1038/nn.3752.

    Article  Google Scholar 

  12. Clark, D. A. (2006). The AFD sensory neurons encode multiple functions underlying thermotactic behavior in caenorhabditis elegans. Journal of Neuroscience, 26, 7444–7451. doi:10.1523/JNEUROSCI.1137-06.2006.

    Article  Google Scholar 

  13. Clark, D. A., Gabel, C. V., Gabel, H., & Samuel, A. D. T. (2007). Temporal activity patterns in thermosensory neurons of freely moving caenorhabditis elegans encode spatial thermal gradients. Journal of Neuroscience, 27, 6083–6090. doi:10.1523/JNEUROSCI.1032-07.2007.

    Article  Google Scholar 

  14. Davis, M. W., Morton, J. J., Carroll, D., & Jorgensen, E. M. (2008). Gene activation using FLP recombinase in C. elegans. PLoS Genetics, 4, e1000028. doi:10.1371/journal.pgen.1000028.

    Article  Google Scholar 

  15. Deisseroth, K. (2010). Optogenetics. Nature Methods, 8, 26–29. doi:10.1038/nmeth.f.324.

    Article  Google Scholar 

  16. Fang-Yen, C., Gabel, C. V., Samuel, A. D. T., et al. (2012). Laser microsurgery in caenorhabditis elegans. In: J. H. Rothman & A. Singson (Eds.), Caenorhabditis elegans: Cell biology and physiology (pp 177–206). Waltham: Elsevier.

    Google Scholar 

  17. Faumont, S. (2006). The awake behaving worm: simultaneous imaging of neuronal activity and behavior in intact animals at millimeter scale. Journal of neurophysiology, 95, 1976–1981. doi:10.1152/jn.01050.2005.

    Article  Google Scholar 

  18. Faumont, S., Rondeau, G., Thiele, T. R., et al. (2011). An image-free opto-mechanical system for creating virtual environments and imaging neuronal activity in freely moving caenorhabditis elegans. PLoS ONE, 6, e24666. doi:10.1371/journal.pone.0024666.

    Article  Google Scholar 

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

    Article  Google Scholar 

  20. Guo, Z. V., Hart, A. C., & Ramanathan, S. (2009). Optical interrogation of neural circuits in Caenorhabditis elegans. Nature Methods, 6, 891–896. doi:10.1038/nmeth.1397.

    Article  Google Scholar 

  21. Han, X., & Boyden, E. S. (2007). Multiple-color optical activation, silencing, and desynchronization of neural activity, with single-spike temporal resolution. PLoS ONE, 2, e299. doi:10.1371/journal.pone.0000299.

    Article  Google Scholar 

  22. Hendricks, M., Ha, H., Maffey, N., & Zhang, Y. (2012). Compartmentalized calcium dynamics in a C. elegans interneuron encode head movement. Nature. doi:10.1038/nature11081.

    Google Scholar 

  23. Hilliard, M. A., Apicella, A. J., Kerr, R., et al. (2004). In vivo imaging of C. elegans ASH neurons: Cellular response and adaptation to chemical repellents. The EMBO Journal, 24, 63–72. doi:10.1038/sj.emboj.7600493.

    Article  Google Scholar 

  24. Holekamp, T. F., Turaga, D., & Holy, T. E. (2008). Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy. Neuron, 57, 661–672. doi:10.1016/j.neuron.2008.01.011.

    Article  Google Scholar 

  25. Husson, S. J., Gottschalk, A., & Leifer, A. M. (2013). Optogenetic manipulation of neural activity in C. elegans: From synapse to circuits and behaviour. Biology Cell, 105, 235–250. doi:10.1111/boc.201200069.

    Article  Google Scholar 

  26. Iino, Y., & Yoshida, K. (2009). Parallel use of two behavioral mechanisms for chemotaxis in caenorhabditis elegans. Journal of Neuroscience, 29, 5370–5380. doi:10.1523/JNEUROSCI.3633-08.2009.

    Article  Google Scholar 

  27. Inagaki, H. K., Jung, Y., Hoopfer, E. D., et al. (2014). Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nature Methods, 11, 325–332. doi:10.1038/nmeth.2765.

    Article  Google Scholar 

  28. Jarrell, T. A., Wang, Y., Bloniarz, A. E., et al. (2012). The connectome of a decision-making neural network. Science, 337, 437–444. doi:10.1126/science.1221762.

    Article  ADS  Google Scholar 

  29. Kato, S., Xu, Y., Cho, C. E., et al. (2014). Temporal responses of C. elegans chemosensory neurons are preserved in behavioral dynamics. Neuron, 81, 616–628. doi:10.1016/j.neuron.2013.11.020.

    Article  Google Scholar 

  30. Kawano, T., Po, M. D., Gao, S., et al. (2011). An imbalancing act: Gap junctions reduce the backward motor circuit activity to bias C. elegans for forward locomotion. Neuron, 72, 572–586. doi:10.1016/j.neuron.2011.09.005.

    Article  Google Scholar 

  31. Kerr, R., Lev-Ram, V., Baird, G., et al. (2000). Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron, 26, 583–594. doi:10.1016/S0896-6273(00)81196-4.

    Article  Google Scholar 

  32. Kimura, K. D., Miyawaki, A., Matsumoto, K., & Mori, I. (2004). The C. elegans thermosensory neuron AFD responds to warming. Current Biology, 14, 1291–1295. doi:10.1016/j.cub.2004.06.060.

    Article  Google Scholar 

  33. Klapoetke, N. C., Murata, Y., Kim, S. S., et al. (2014). Independent optical excitation of distinct neural populations. Nature Methods, 11, 338–346. doi:10.1038/nmeth.2836.

    Article  Google Scholar 

  34. Kocabas, A., Shen, C.-H., Guo, Z. V., & Ramanathan, S. (2012). Controlling interneuron activity in Caenorhabditis elegans to evoke chemotactic behaviour. Nature, 490, 273–277. doi:10.1038/nature11431.

    Article  ADS  Google Scholar 

  35. Larsch, J., Ventimiglia, D., Bargmann, C. I., & Albrecht, D. R. (2013). High-throughput imaging of neuronal activity in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 110, E4266–E4273. doi:10.1073/pnas.1318325110.

    Article  Google Scholar 

  36. Leifer, A. M., Fang-Yen, C., Gershow, M., Alkema, M. J., & Samuel, A. D. T. (2011). Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nat Meth, 8(2), 147–152. doi: 10.1038/nmeth.1554

    Google Scholar 

  37. Looger, L. L., & Griesbeck, O. (2012). Genetically encoded neural activity indicators. Current Opinion in Neurobiology, 22, 18–23. doi:10.1016/j.conb.2011.10.024.

    Article  Google Scholar 

  38. Luo, L., Cook, N., Venkatachalam, V., et al. (2014a). Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons. Proceedings of the National Academy of Sciences of the United States of America, 111, 2776–2781. doi:10.1073/pnas.1315205111.

    Google Scholar 

  39. Luo, L., Wen, Q., Ren, J., et al. (2014b). Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit. Neuron, 82, 1115–1128. doi:10.1016/j.neuron.2014.05.010.

    Google Scholar 

  40. Macosko, E. Z., Pokala, N., Feinberg, E. H., et al. (2009). A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature, 458, 1171–1175. doi:10.1038/nature07886.

    Article  ADS  Google Scholar 

  41. McCormick, K. E., Gaertner, B. E., Sottile, M., et al. (2011). Microfluidic devices for analysis of spatial orientation behaviors in Semi-Restrained caenorhabditis elegans. PLoS ONE, 6, e25710. doi:10.1371/journal.pone.0025710.

    Article  Google Scholar 

  42. Miyawaki, A., Griesbeck, O., Heim, R., & Tsien, R. Y. (1999). Dynamic and quantitative Ca2 + measurements using improved cameleons. Proceedings of the National Academy of Sciences of the United States of America, 96, 2135–2140. doi:10.1073/pnas.96.5.2135.

    Article  ADS  Google Scholar 

  43. Miyawaki, A., Llopis, J., Heim, R., McCaffery, J. M., Adams, J. A., Ikura, M., & Tsien, R. Y. (1997). Fluorescent indicators for Ca2+based on green fluorescent proteins and calmodulin. Nature, 388(6645), 882–887.

    Google Scholar 

  44. Miyawaki, A., Llopis, J., Heim, R., et al. (2007). Fluorescent indicators for Ca2 + based on green fluorescent proteins and calmodulin. Nature, 388, 882–887. doi:10.1038/42264.

    ADS  Google Scholar 

  45. Nagel, G., Brauner, M., Liewald, J. F., et al. (2005). Light activation of channelrhodopsin-2 in excitable cells of caenorhabditis elegans triggers rapid behavioral responses. Current Biology, 15, 2279–2284. doi:10.1016/j.cub.2005.11.032.

    Article  Google Scholar 

  46. Piggott, B. J., Liu, J., Feng, Z., et al. (2011). The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans. Cell, 147, 922–933. doi:10.1016/j.cell.2011.08.053.

    Article  Google Scholar 

  47. Prevedel, R., Yoon, Y.-G., Hoffmann, M., Pak, N., Wetzstein, G., Kato, S.,… Vaziri, A. (2014). Simultaneous whole-animal 3D imaging of neuronal activity using light-field microscopy. Nat Meth, 11(7), 727–730. doi: 10.1038/nmeth.2964

    Google Scholar 

  48. Qi, Y. B., Garren, E. J., Shu, X., et al. (2012). Photo-inducible cell ablation in Caenorhabditis elegans using the genetically encoded singlet oxygen generating protein miniSOG. Proceedings of the National Academy of Sciences of the United States of America, 109, 7499–7504. doi:10.1073/pnas.1204096109.

    Article  ADS  Google Scholar 

  49. Richmond, J. E., & Jorgensen, E. M. (1999). Nature Neuroscience, 2, 791–797. doi:10.1038/12160.

    Article  Google Scholar 

  50. Schrödel, T., Prevedel, R., Aumayr, K., et al. (2013). Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light. Nature Methods, 10, 1013–1020. doi:10.1038/nmeth.2637.

    Article  Google Scholar 

  51. Shipley, F. B., Clark, C. M., Alkema, M. J., & Leifer, A. M. (2014). Simultaneous optogenetic manipulation and calcium imaging in freely moving C. elegans. Front Neural Circuits, 8, 28. doi:10.3389/fncir.2014.00028.

    Article  Google Scholar 

  52. Stetina Von, S. E., Treinin, M., & Miller, D. M. III. (2005). The motor circuit. In E. J. Aamodt (Ed.), The neurobiology of C. elegans (pp. 125–167). San Diego: Elsevier.

    Google Scholar 

  53. Stirman, J. N., Crane, M. M., Husson, S. J., Wabnig, S., Schultheis, C., Gottschalk, A., & Lu, H. (2011). Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nat Meth, 8(2), 153–158. doi: 10.1038/nmeth.1555

    Google Scholar 

  54. Sulston, J. E., & Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Developmental Biology, 56, 110–156. doi:10.1016/0012-1606(77)90158-0.

    Article  Google Scholar 

  55. Sulston, J. E., Schierenberg, E., White, J. G., & Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology, 100, 64–119. doi:10.1016/0012-1606(83)90201-4.

    Article  Google Scholar 

  56. Suzuki, H., Kerr, R., Bianchi, L., et al. (2003a). In Vivo Imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 Channel in the process of gentle touch sensation. Neuron, 39, 1005–1017. doi:10.1016/j.neuron.2003.08.015.

    Google Scholar 

  57. Suzuki, H., Kerr, R., Bianchi, L., et al. (2003b). In Vivo Imaging of C. elegans mechanosensory neurons demonstrates a specific role for the MEC-4 channel in the process of gentle touch sensation. Neuron, 39, 1005–1017. doi:10.1016/j.neuron.2003.08.015.

    Google Scholar 

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

    Article  ADS  Google Scholar 

  59. Wen, Q., Po, M. D., Hulme, E., et al. (2012). Proprioceptive coupling within motor neurons drives C. elegans forward kocomotion. Neuron, 76, 750–761. doi:10.1016/j.neuron.2012.08.039.

    Article  Google Scholar 

  60. White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986). The structure of the nervous system of the nematode caenorhabditis elegans. Philosophical Transactions of the Royal Society of London B Biological Science, 314, 1–340. doi:10.1098/rstb.1986.0056.

    Article  ADS  Google Scholar 

  61. Williams, D. C., Bejjani El, R., Ramirez, P. M., et al. (2013). Rapid and permanent neuronal inactivation in vivo via subcellular generation of reactive oxygen with the use of KillerRed. Cell Reports, 5, 553–563. doi:10.1016/j.celrep.2013.09.023.

    Article  Google Scholar 

  62. Wu, Y., Ghitani, A., Christensen, R., et al. (2011). Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 108, 17708–17713. doi:10.1073/pnas.1108494108.

    Article  ADS  Google Scholar 

  63. Zhang, F., Wang, L.-P., Brauner, M., et al. (2007). Multimodal fast optical interrogation of neural circuitry. Nature, 446, 633–639. doi:10.1038/nature05744.

    Article  ADS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Key Laboratory of Modern Acoustics, Ministry of Education, Department of Physics, Nanjing University, 210093, Nanjing, China

    Linjiao Luo

  2. Department of Neurobiology and Biophysics, School of Life Sciences, University of Science and Technology of China, Hefei, Anhui Province, China

    Quan Wen

  3. Department of Physics and Center for Brain Science, Harvard University, 02138, Cambridge, MA, USA

    Aravinthan D. T. Samuel

Authors
  1. Linjiao Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Quan Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aravinthan D. T. Samuel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aravinthan D. T. Samuel .

Editor information

Editors and Affiliations

  1. Dept. Of Neurobiology and Anatomy, University of Utah, Salt Lake City, Utah, USA

    Adam D. Douglass

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Luo, L., Wen, Q., Samuel, A. (2015). Optically Monitoring and Manipulating Brain and Behavior in C. elegans . In: Douglass, A. (eds) New Techniques in Systems Neuroscience. Biological and Medical Physics, Biomedical Engineering. Springer, Cham. https://doi.org/10.1007/978-3-319-12913-6_7

Download citation

Publish with us

Policies and ethics

Search

Navigation