Caenorhabditis elegans: a model system for systems neuroscience

Current Opinion in Neurobiology

Volumn 19, Issue 6, 2009, Pages 637-643

  Sengupta, Piali ^a   Samuel, Aravinthan DT ^b  

^a BRANDEIS UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; BEHAVIORAL SCIENCE; BIOLOGICAL MODEL; CAENORHABDITIS ELEGANS; INTERNEURON; LOCOMOTION; MOTOR CONTROL; MOTOR SYSTEM; NERVE CELL PLASTICITY; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NEUROMODULATION; NEUROSCIENCE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVIEW; SENSORY STIMULATION; STIMULUS RESPONSE;

ANIMALS; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; HUMANS; MODELS, NEUROLOGICAL; NEUROSCIENCES;

EID: 72549086503     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2009.09.009     Document Type: Review

References (62)

1. Marder E., and Calabrese R.L. Principles of rhythmic motor pattern generation. Physiol Rev 76 (1996) 687-717
2. Grillner S., Kozlov A., Dario P., Stefanini C., Menciassi A., Lansner A., and Hellgren Kotaleski J. Modeling a vertebrate motor system: pattern generation, steering and control of body orientation. Prog Brain Res 165 (2007) 221-234
3. White J.G., Southgate E., Thomson J.N., and Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B 314 (1986) 1-340
4. Chen B.L., Hall D.H., and Chklovskii D.B. Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci U S A 103 (2006) 4723-4728. The layout of the worm nervous system could be derived from first principles using the concept of wire minimization, reducing the amount of neuronal fiber that is required to produce the pattern of synaptic connectivity in worm neuronal circuits. Additional synaptic connectivity that was not completed in the original wiring diagram was found in the motor circuit.
5. Pierce-Shimomura J.T., Chen B.L., Mun J.J., Ho R., Sarkis R., and McIntire S.L. Genetic analysis of crawling and swimming locomotory patterns in C. elegans. Proc Natl Acad Sci U S A 105 (2008) 20982-20987
6. Croll N.A. The Behavior of Nematodes (1970), St. Martin's, New York
7. Berri S., Boyle J.H., Tassieri M., Hope I.A., and Cohen N. Forward locomotion of the nematode C. elegans is achieved through modulation of a single gait. HFSP J 3 (2009) 186-193. Worms swim in fluids and crawl on solid surfaces with distinct locomotory gaits. By putting worms in environments that posed intermediate amounts of mechanical load, it was shown that the worm continuously adjusts its gait between the extremes of swimming and crawling.
8. Wallace H.R. Movement of eelworms II: a comparative study of the movement in soil of Heterodera schachtii schmidt and of Ditylenchus dipsaci (Kuhn) Filipjev. Ann Appl Biol 46 (1958) 86-94
9. Bryden J., and Cohen N. Neural control of Caenorhabditis elegans forward locomotion: the role of sensory feedback. Biol Cybern 98 (2008) 339-351
10. Korta J., Clark D.A., Gabel C.V., Mahadevan L., and Samuel A.D. Mechanosensation and mechanical load modulate the locomotory gait of swimming C. elegans. J Exp Biol 210 (2007) 2383-2389
11. Karbowski J., Schindelman G., Cronin C.J., Seah A., and Sternberg P.W. Systems level circuit model of C. elegans undulatory locomotion: mathematical modeling and molecular genetics. J Comput Neurosci 24 (2008) 253-276
12. Boyle J.H., and Cohen N. Caenorhabditis elegans body wall muscles are simple actuators. Biosystems 94 (2008) 170-181
13. Kerr R., Lev-Ram V., Baird G., Vincent P., Tsien R.Y., and Schafer W.R. Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26 (2000) 583-594
14. Zhang F., Wang L.P., Brauner M., Liewald J.F., Kay K., Watzke N., Wood P.G., Bamberg E., Nagel G., Gottschalk A., et al. Multimodal fast optical interrogation of neural circuitry. Nature 446 (2007) 633-639
15. Nagel G., Brauner M., Liewald J.F., Adeishvili N., Bamberg E., and Gottschalk A. Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses. Curr Biol 15 (2005) 2279-2284
16. Liewald J.F., Brauner M., Stephens G.J., Bouhours M., Schultheis C., Zhen M., and Gottschalk A. Optogenetic analysis of synaptic function. Nat Methods 5 (2008) 895-902. Optogenetic techniques were devised to manipulate neurotransmission between specific cell types in the motor circuit of freely moving worms, providing bidirectional optical control to contract or relax the muscles that drive locomotion.
17. Liu Q., Hollopeter G., and Jorgensen E.M. Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction. Proc Natl Acad Sci U S A 106 (2009) 10823-10828. Simultaneous electrical recording of muscle cells and optogenetic stimulation of motor neurons showed that synaptic transmission at the neuromuscular junction varies continuously in strength. Thus, the motor circuit operates as an analog device.
18. Farah N., Reutsky I., and Shoham S. Patterned optical activation of retinal ganglion cells. Proceedings of the 29th Annual International Conference on IEEE EMBS. Lyon, France (2007) 6368-6370
19. Zheng Y., Brockie P.J., Mellem J.E., Madsen D.M., and 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 (1999) 347-361
20. Brockie P.J., Mellem J.E., Hills T., Madsen D.M., and Maricq A.V. The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion. Neuron 31 (2001) 617-630
21. Chalfie M., Sulston J.E., White J.G., Southgate E., Thomson J.N., and Brenner S. The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5 (1985) 956-964
22. Stephens G.J., Johnson-Kerner B., Bialek W., and Ryu W.S. Dimensionality and dynamics in the behavior of C. elegans. PLoS Comput Biol 4 (2008) e1000028. The detailed postures of freely crawling worms were analyzed at high resolution using a tracking microscope, and discovered to be describable using a small number of dimensions. Despite the large number of individual components in the motor circuit, motor control in the worm is achieved through a small number of degrees of freedom.
23. Srivastava N., Clark D.A., and Samuel A.D. Temporal analysis of stochastic turning behavior of swimming C. elegans. J Neurophysiol 102 (2009) 1172-1179. The spontaneous turning movements of individual swimming worms were quantified over long periods of time, and shown to be describable using a simple Markov model involving two run states, with distinct probabilities of transition to the turn state.
24. Faumont S., and Lockery S.R. The awake behaving worm: simultaneous imaging of neuronal activity and behavior in intact animals at millimeter scale. J Neurophysiol 95 (2006) 1976-1981
25. Clark D.A., Gabel C.V., Gabel H., and Samuel A.D. Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients. J Neurosci 27 (2007) 6083-6090. A tracking microscope was used to follow calcium transients within individual thermosensory neurons of worms navigating temperature gradients, allowing simultaneous measurements of unrestrained behavior and neuronal activity.
26. Chronis N., Zimmer M., and Bargmann C.I. Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat Methods 4 (2007) 727-731. Intracellular calcium dynamics in the AVA command interneurons were correlated with initiation and duration of forward propagating waves by trapping worms in microfluidics devices. These devices also permit optical imaging of sensory neurons in the absence of confounding variables of other immobilization methods.
27. Dusenbery D.B. Analysis of chemotaxis in the nematode Caenorhabditis elegans by countercurrent separation. J Exp Zool 188 (1974) 41-47
28. Ryu W.S., and Samuel A.D. Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined thermal stimuli. J Neurosci 22 (2002) 5727-5733
29. Luo L., Gabel C.V., Ha H.I., Zhang Y., and Samuel A.D. Olfactory behavior of swimming C. elegans analyzed by measuring motile responses to temporal variations of odorants. J Neurophysiol 99 (2008) 2617-2625. An olfactory assay was designed for swimming worms that allowed precise and robust quantification of attractive and repulsive olfactory responses with single worm resolution.
30. Luo L., Clark D.A., Biron D., Mahadevan L., and Samuel A.D. Sensorimotor control during isothermal tracking in Caenorhabditis elegans. J Exp Biol 209 (2006) 4652-4662
31. Zariwala H.A., Miller A.C., Faumont S., and Lockery S.R. Step response analysis of thermotaxis in Caenorhabditis elegans. J Neurosci 23 (2003) 4369-4377
32. Pierce-Shimomura J.T., Morse T.M., and Lockery S.R. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J Neurosci 19 (1999) 9557-9569
33. Ramot D., MacInnis B.L., Lee H.C., and Goodman M.B. Thermotaxis is a robust mechanism for thermoregulation in Caenorhabditis elegans nematodes. J Neurosci 28 (2008) 12546-12557
34. Berg H.C., and Brown D.A. Chemotaxis in E. coli analysed by three-dimensional tracking. Nature 239 (1972) 500-504
35. Wakabayashi T., Kitagawa I., and Shingai R. Neurons regulating the duration of forward locomotion in Caenorhabditis elegans. Neurosci Res 50 (2004) 103-111
36. Gray J.M., Hill J.J., and Bargmann C.I. A circuit for navigation in Caenorhabditis elegans. Proc Natl Acad Sci U S A 102 (2005) 3184-3191
37. Hills T., Brockie P.J., and Maricq A.V. Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J Neurosci 24 (2004) 1217-1225
38. Tsalik E.L., and Hobert O. Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. J Neurobiol 56 (2003) 178-197
39. Chalasani S.H., Chronis N., Tsunozaki M., Gray J.M., Ramot D., Goodman M.B., and Bargmann C.I. Dissecting a neural circuit for food-seeking behavior in Caenorhabditis elegans. Nature 450 (2007) 63-70. Imaging of temporal dynamics of intracellular calcium responses described information flow between the AWC sensory neurons, and their postsynaptic partners, the AIY and AIB interneurons. Removal of olfactory stimuli activates the AWC and AIB neurons, but inhibits the AIY interneurons. The parallel ON/OFF channels of stimulus transmission through the circuit may regulate the generation of probabilistic navigation behavior.
40. Suzuki H., Thiele T.R., Faumont S., Ezcurra M., Lockery S.R., and Schafer W.R. Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature 454 (2008) 114-117. Navigation on a salt gradient is regulated by asymmetric sensory responses in the ASE chemosensory neurons. The left ASE neuron responds to upsteps in salt concentration and lengthens runs, whereas the right ASE neuron responds to salt downsteps and increases turns. ON/OFF information from the left and right ASE neurons converges downstream to provide a time derivative of the salt concentration.
41. Hilliard M.A., Apicella A.J., Kerr R., Suzuki H., Bazzicalupo P., and Schafer W.R. In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. EMBO J 24 (2005) 63-72
42. Kimura K.D., Miyawaki A., Matsumoto K., and Mori I. The C. elegans thermosensory neuron AFD responds to warming. Curr Biol 14 (2004) 1291-1295
43. Clark D.A., Biron D., Sengupta P., and Samuel A.D.T. The AFD sensory neurons encode multiple functions underlying thermotactic behavior in C. elegans. J Neurosci 26 (2006) 7444-7451. The stimulus-response properties of the AFD thermosensory neuron were mapped using calcium imaging and subjecting worms to a wide range of temperature waveforms. AFD responds to both increases and decreases in temperature, effectively calculating the time derivative of thermosensory input, and the temperature range of its sensitivity encodes thermotactic memory.
44. Zimmer M., Gray J.M., Pokala N., Chang A.J., Karow D.S., Marletta M.A., Hudson M.L., Morton D.B., Chronis N., and Bargmann C.I. Neurons detect increases and decreases in oxygen levels using distinct guanylate cyclases. Neuron 61 (2009) 865-879. Sensory neurons sense increases or decreases in ambient oxygen levels with distinct temporal dynamics, and contribute to the different locomotory behaviors exhibited by C. elegans upon shifts away from, or toward, its preferred oxygen concentration.
45. Persson A., Gross E., Laurent P., Busch K.E., Bretes H., and de Bono M. Natural variation in a neural globin tunes oxygen sensing in wild Caenorhabditis elegans. Nature 458 (2009) 1030-1033. Sensory neurons sense increases or decreases in ambient oxygen levels with distinct temporal dynamics, and contribute to the different locomotory behaviors exhibited by C. elegans upon shifts away from, or toward, its preferred oxygen concentration.
46. Biron D., Wasserman S.M., Thomas J.H., Samuel A.D., and Sengupta P. An olfactory neuron responds stochastically to temperature and modulates C. elegans thermotactic behavior. Proc Natl Acad Sci U S A 105 (2008) 11002-11007. The AWC sensory neurons respond stochastically, but in a stimulus-correlated manner to thermal stimuli and contribute to turning behavior on thermal gradients. Deterministic responses of the AFD thermosensory neuron type and stochastic responses of the AWC neurons to thermal stimuli may be integrated downstream in the circuit to regulate navigation on spatial thermal gradients.
47. Iino Y., and Yoshida K. Parallel use of two behavioral mechanisms for chemotaxis in Caenorhabditis elegans. J Neurosci 29 (2009) 5370-5380. When C. elegans navigates chemical gradients, it not only modulates the rate of abrupt turns to execute a biased random walk, but also gradually steers the direction of its runs to orient itself toward its navigational goals. Simulations show that this additional sophistication in behavioral strategy is an integral part of the fidelity of C. elegans chemotaxis.
48. Hedgecock E.M., and Russell R.L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 72 (1975) 4061-4065
49. Mori I., and Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376 (1995) 344-348
50. Cheung B.H., Cohen M., Rogers C., Albayram O., and de Bono M. Experience-dependent modulation of C. elegans behavior by ambient oxygen. Curr Biol 15 (2005) 905-917
51. Gray J.M., Karow D.S., Lu H., Chang A.J., Chang J.S., Ellis R.E., Marletta M.A., and Bargmann C.I. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430 (2004) 317-322
52. Dunn N.A., Conery J.S., and Lockery S.R. Circuit motifs for spatial orientation behaviors identified by neural network optimization. J Neurophysiol 98 (2007) 888-897. Optimum computational strategies were derived in C. elegans for climbing spatial gradients or for remaining within a particular location in the environment based on calculations that could be carried out by motifs in the neural circuits for navigation.
53. Saeki S., Yamamoto M., and Iino Y. Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J Exp Biol 204 (2001) 1757-1764
54. Tomioka M., Adachi T., Suzuki H., Kunitomo H., Schafer W.R., and Iino Y. The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51 (2006) 613-625. Prolonged exposure to a normally attractive salt stimulus paired with starvation results in avoidance of salt upon subsequent exposure. This plasticity is mediated via insulin secretion from an interneuron which feeds back on a salt-sensing neuron (ASER) that senses downsteps in salt concentration to modulate its functions and alter navigation behavior.
55. Ishihara T., Iino Y., Mohri A., Mori I., Gengyo-Ando K., Mitani S., and Katsura I. HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans. Cell 109 (2002) 639-649
56. Hukema R.K., Rademakers S., Dekkers M.P., Burghoorn J., and Jansen G. Antagonistic sensory cues generate gustatory plasticity in Caenorhabditis elegans. EMBO J 25 (2006) 312-322
57. Zhang Y., Lu H., and Bargmann C.I. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438 (2005) 179-184
58. Chao M.Y., Komatsu H., Fukuto H.S., Dionne H.M., and Hart A.C. Feeding status and serotonin rapidly and reversibly modulate a Caenorhabditis elegans chemosensory circuit. Proc Natl Acad Sci U S A 101 (2004) 15512-15517
59. Kano T., Brockie P.J., Sassa T., Fujimoto H., Kawahara Y., Iino Y., Mellem J.E., Madsen D.M., Hosono R., and Maricq A.V. Memory in Caenorhabditis elegans is mediated by NMDA-type ionotropic glutamate receptors. Curr Biol 18 (2008) 1010-1015
60. Harris G.P., Hapiak V.M., Wragg R.T., Miller S.B., Hughes L.J., Hobson R.J., Steven R., Bamber B., and Komuniecki R.W. Three distinct amine receptors operating at different levels within the locomotory circuit are each essential for the serotonergic modulation of chemosensation in Caenorhabditis elegans. J Neurosci 29 (2009) 1446-1456
61. Tsunozaki M., Chalasani S.H., and Bargmann C.I. A behavioral switch: cGMP and PKC signaling in olfactory neurons reverses odor preference in C. elegans. Neuron 59 (2008) 959-971. Mutations in an AWC sensory neuron-expressed receptor guanylyl cyclase and PKC result in avoidance of a normally attractive olfactory stimulus. Although sensory responses are unaffected by these mutations, these molecules may act to regulate the synaptic output of one of the bilateral AWC neuron pair in an experience-dependent manner to direct avoidance or attraction behavior. Thus, altered activity of a single sensory neuron can switch olfactory preferences via effects on navigational strategy.
62. Macosko E.Z., Pokala N., Feinberg E.H., Chalasani S.H., Butcher R.A., Clardy J., and Bargmann C.I. A hub-and-spoke circuit drives pheromone attraction and social behavior in C. elegans. Nature 458 (2009) 1171-1175