Behavioral plasticity in C. elegans: Paradigms, circuits, genes

Journal of Neurobiology

Volumn 54, Issue 1, 2003, Pages 203-223

  Hobert, Oliver ^a  

^a College of Physicians and Surgeons ^*  (United States)

Author keywords

Behavioral plasticity; C. elegans; Circuits; Genes

Indexed keywords

ION CHANNEL; NEUROPEPTIDE; NEUROTRANSMITTER; NEUROTRANSMITTER RECEPTOR; TRANSCRIPTION FACTOR;

BEHAVIOR GENETICS; CAENORHABDITIS ELEGANS; CHEMOTAXIS; DEFECATION; DOWNSTREAM PROCESSING; EGG LAYING; EXPERIMENTAL MODEL; FEEDING BEHAVIOR; GENE FUNCTION; GENETIC ANALYSIS; GENOME; HABITUATION; LOCOMOTION; MATING; MECHANORECEPTOR; MICROBIAL GENETICS; MOTOR ACTIVITY; MOTOR CONTROL; MUSCLE CONTRACTION; NERVE CELL; NERVE CELL PLASTICITY; NERVOUS SYSTEM; NONHUMAN; ODOR; PHARYNX; PRIORITY JOURNAL; PROPRIOCEPTION; REVIEW; SENSORY STIMULATION; SKIN SENSATION; SOIL; STATE DEPENDENT LEARNING;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ASSOCIATION LEARNING; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CHEMOTAXIS; GENETICS, BEHAVIORAL; GENOME; HABITUATION, PSYCHOPHYSIOLOGIC; LOCOMOTION; MECHANICS; MODELS, BIOLOGICAL; MOTOR ACTIVITY; MUTATION; NERVE NET; NERVOUS SYSTEM PHYSIOLOGY; NEURONAL PLASTICITY; NEURONS; SEQUENCE HOMOLOGY, AMINO ACID; SEROTONIN; SIGNAL TRANSDUCTION; TEMPERATURE;

EID: 0037219784     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/neu.10168     Document Type: Review

References (104)

1. Abel T, Kandel E. 1998. Positive and negative regulatory mechanisms that mediate long-term memory storage. Brain Res Brain Res Rev 26:360-378.
2. Abel T, Martin KC, Bartsch D, Kandel ER. 1998. Memory suppressor genes: Inhibitory constraints on the storage of long-term memory. Science 279:338-341.
3. Avery L, Horvitz HR. 1990. Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J Exp Zool 253:263-270.
4. Avery L, Bargmann CI, Horvitz HR. 1993. The Caenorhabditis elegans UNC-31 gene affects multiple nervous system-controlled functions. Genetics 134:455-464.
5. Avery L, Thomas JH. 1997. Feeding and defecation. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C. elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, p 679-716.
6. Baek J, Cosman P, Feng Z, Silver J, Schafer W. 2002. Using machine vision to analyze and classify Caenorhabditis elegans behavioral phenotypes quantitatively. J Neurosci Methods 118:9-21.
7. Bargmann CI. 1998. Neurobiology of the Caenorhabditis elegans genome. Science 282:2028-2033.
8. Bargmann CI, Kaplan JM. 1998. Signal transduction in the Caenorhabditis elegans nervous system. Annu Rev Neurosci 21:279-308.
9. Bargmann CI, Hartwieg E, Horvitz HR. 1993. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74:515-527.
10. Bellocchio EE, Reimer RJ, Fremeau RT Jr, Edwards RH. 2000. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289:957-960.
11. Benzer S. 1967. Behavioral mutants of Drosophila isolated by counter-current distribution. Proc Natl Acad Sci USA 58:1112-1119.
12. Berger AJ, Hart AC, Kaplan JM. 1998. G alphas-induced neurodegeneration in Caenorhabditis elegans. J Neurosci 18:2871-2880.
13. Berwin B, Floor E, Martin TF. 1998. CAPS (mammalian UNC-31) protein localizes to membranes involved in dense-core vesicle exocytosis. Neuron 21:137-145.
14. Bessereau JL, Wright A, Williams DC, Schuske K, Davis MW, Jorgensen EM. 2001. Mobilization of a Drosophila transposon in the Caenorhabditis elegans germ line. Nature 413:70-74.
15. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
16. Brockie PJ, Madsen DM, Zheng Y, Mellem J, Maricq AV. 2001a. Differential expression of glutamate receptor subunits in the nervous system of Caenorhabditis elegans and their regulation by the homeodomain protein UNC-42. J Neurosci 21:1510-1522.
17. Brockie PJ, Mellem JE, Hills T, Madsen DM, Maricq AV. 2001b. The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion. Neuron 31:617-630.
18. Cassata G, Kuhn F, Witmer A, Kirchhofer R, Burglin TR. 2000. A steep thermal gradient thermotaxis assay for the nematode Caenorhabditis elegans. Genesis 27:141-144.
19. Chalfie M, Au M. 1989. Genetic control of differentiation of the Caenorhabditis elegans touch receptor neurons. Science 243:1027-1033.
20. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S. 1985. The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5:956-964.
21. Colbert HA, Bargmann CI. 1995. Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14:803-812.
22. Colbert HA, Bargmann CI. 1997. Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. Learn Mem 4:179-191.
23. Colbert HA, Smith TL, Bargmann CI. 1997. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17: 8259-8269.
24. Dal Santo P, Logan MA, Chisholm AD, Jorgensen EM. 1999. The inositol trisphosphate receptor regulates a 50-second behavioral rhythm in C. elegans. Cell 98:757-767.
25. Davis RL. 1996. Physiology and biochemistry of Drosophila learning mutants. Physiol Rev 76:299-317.
26. de Belle JS, Heisenberg M. 1996. Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: A case study of the mushroom body miniature gene (mbm). Proc Natl Acad Sci USA 93:9875-9880.
27. Driscoll M, Kaplan J. 1997. Mechanotransduction. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C. elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, p 645-678.
28. Elkes DA, Cardozo DL, Madison J, Kaplan JM. 1997. EGL-36 Shaw channels regulate C. elegans egg-laying muscle activity. Neuron 19:165-174.
29. Ferree TC, Lockery SR. 1999. Computational rules for chemotaxis in the nematode C. elegans. J Comput Neurosci 6:263-277.
30. Gems D, Riddle DL. 2000. Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans. Genetics 154:1597-1610.
31. Gerlai R. 1996. Gene-targeting studies of mammalian behavior: Is it the mutation or the background genotype? Trends Neurosci 19:177-181.
32. Gomez M, De Castro E, Guarin E, Sasakura H, Kuhara A, Mori I, Bartfai T, Bargmann CI, Nef P. 2001. Ca(2+) Signaling via the neuronal calcium sensor-1 regulates associative learning and memory in C. elegans. Neuron 30:241-248.
33. Goodman MB, Hall DH, Avery L, Lockery SR. 1998. Active currents regulate sensitivity and dynamic range in C. elegans neurons. Neuron 20:763-772.
34. Greenspan RJ. 1997. A kinder, gentler genetic analysis of behavior: Dissection gives way to modulation. Curr Opin Neurobiol 7:805-811.
35. Greenspan RJ. 2001. The flexible genome. Nat Rev Genet 2:383-387.
36. Griffith LC, Verselis LM, Aitken KM, Kyriacou CP, Danho W, Greenspan RJ. 1993. Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila disrupts behavioral plasticity. Neuron 10:501-509.
37. Harbinder S, Tavernarakis N, Herndon LA, Kinnell M, Xu SQ, Fire A, Driscoll M. 1997. Genetically targeted cell disruption in Caenorhabditis elegans. Proc Natl Acad Sci USA 94:13128-13133.
38. Hardaker LA, Singer E, Kerr R, Zhou G, Schafer WR. 2001. Serotonin modulates locomotory behavior and coordinates egg-laying and movement in Caenorhabditis elegans. J Neurobiol 49:303-313.
39. Hart AC, Sims S, Kaplan JM. 1995. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378:82-85.
40. Hedgecock EM, Culotti JG, Hall DH. 1990. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4:61-85.
41. Hedgecock EM, Russell RL. 1975. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 72:4061-4065.
42. Heisenberg M. 1998. What do the mushroom bodies do for the insect brain? an introduction. Learn Mem 5:1-10.
43. Hobert O, Mori I, Yamashita Y, Honda H, Ohshima Y, Liu Y, Ruvkun G. 1997. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19:345-357.
44. Hodgkin J, Doniach T. 1997. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146:149-164.
45. Huang M, Chalfie M. 1994. Gene interactions affecting mechanosensory transduction in Caenorhabditis elegans. Nature 367:467-470.
46. Ishihara T, Iino Y, Mohri A, Mori I, Gengyo-Ando K, Mitani S, Katsura I. 2002. HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans. Cell 109:639-649.
47. Jansen G, Hazendonk E, Thijssen KL, Plasterk RH. 1997. Reverse genetics by chemical mutagenesis in Caenorhabditis elegans. Nat Genet 17:119-121.
48. Jansen G, Weinkove D, Plasterk RH. 2002. The G-protein gamma subunit gpc-1 of the nematode C. elegans is involved in taste adaptation. EMBO J 21:986-994.
49. Johnstone DB, Wei A, Butler A, Salkoff L, Thomas JH. 1997. Behavioral defects in C. elegans egl-36 mutants result from potassium channels shifted in voltage-dependence of activation. Neuron 19:151-164.
50. Kass J, Jacob TC, Kim P, Kaplan JM. 2001. The EGL-3 proprotein convertase regulates mechanosensory responses of Caenorhabditis elegans. J Neurosci 21:9265-9272.
51. Kerr R, Lev-Ram V, Baird G, Vincent P, Tsien RY, Schafer WR. 2000. Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26: 583-594.
52. Korswagen HC, van der Linden AM, Plasterk RH. 1998. G protein hyperactivation of the Caenorhabditis elegans adenylyl cyclase SGS-1 induces neuronal degeneration. EMBO J 17:5059-5065.
53. Kuhara A, Inada H, Katsura I, Mori I. 2002. Negative regulation and gain control of sensory neurons by the C. elegans calcineurin TAX-6. Neuron 33:751-763.
54. Lee RY, Sawin ER, Chalfie M, Horvitz HR, Avery L. 1999. EAT-4, a homolog of a mammalian sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in Caenorhabditis elegans. J Neurosci 19:159-167.
55. L'Etoile ND, Bargmann CI. 2000. Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1. Neuron 25:575-586.
56. Li C, Kim K, Nelson LS. 1999. FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Res 848:26-34.
57. Maricq AV, Peckol E, Driscoll M, Bargmann CI. 1995. Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor. Nature 378:78-81.
58. Minke B, Cook B. 2002. TRP channel proteins and signal transduction. Physiol Rev 82:429-472.
59. Mitani S, Du H, Hall DH, Driscoll M, Chalfie M. 1993. Combinatorial control of touch receptor neuron expression in Caenorhabditis elegans. Development 119:773-783.
60. Mori I. 1999. Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. Annu Rev Genet 33: 399-422.
61. Mori I, Ohshima Y. 1995. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376:344-348.
62. Morrison GE, van der Kooy D. 2001. A mutation in the AMPA-type glutamate receptor, glr-1, blocks olfactory associative and nonassociative learning in Caenorhabditis elegans. Behav Neurosci 115:640-649.
63. Morrison GE, Wen JY, Runciman S, van der Kooy D. 1999. Olfactory associative learning in Caenorhabditis elegans is impaired in lrn-1 and lrn-2 mutants. Behav Neurosci 113:358-367.
64. Nathoo AN, Moeller RA, Westlund BA, Hart AC. 2001. Identification of neuropeptide-like protein gene families in Caenorhabditis elegans and other species. Proc Natl Acad Sci USA 98:14000-14005.
65. Nelson LS, Rosoff ML, Li C. 1998. Disruption of a neuropeptide gene, flp-1, causes multiple behavioral defects in Caenorhabditis elegans, Science 281:1686-1690.
66. Nuttley WM, Harbinder S, van der Kooy D, 2001. Regulation of distinct attractive and aversive mechanisms mediating benzaldehyde chemotaxis in Caenorhabditis elegans. Learn Mem 8:170-181.
67. Pierce SB, Costa M, Wisotzkey R, Devadhar S, Homburger SA, Buchman AR, Ferguson KC, Heller J, Platt DM, Pasquinelli AA, Liu LX, Doberstein SK, Ruvkun G. 2001. Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family, Genes Dev 15: 672-686.
68. Pierce-Shimomura JT, Morse TM, Lockery SR. 1999. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J Neurosci 19:9557-9569.
69. Pitcher JA, Freedman NJ, Lefkowitz RJ. 1998. G proteincoupled receptor kinases. Annu Rev Biochem 67:653-692.
70. Ranganathan R, Cannon SC, Horvitz HR. 2000. MOD-1 is a serotonin-gated chloride channel that modulates locomotory behaviour in C. elegans. Nature 408:470-475.
71. Ranganathan R, Sawin ER, Trent C, Horvitz HR. 2001. Mutations in the Caenorhabditis elegans serotonin reuptake transporter MOD-5 reveal serotonin-dependent and -independent activities of fluoxetine. J Neurosci 21: 5871-5884.
72. Rankin CH. 2000. Context conditioning in habituation in the nematode Caenorhabditis elegans. Behav Neurosci 114:496-505.
73. Rankin CH, Wicks SR. 2000. Mutations of the Caenorhabditis elegans brain-specific inorganic phosphate transporter eat-4 affect habituation of the tap-withdrawal response without affecting the response itself. J Neurosci 20:4337-4344.
74. Rankin CH, Beck CD, Chiba CM. 1990. Caenorhabditis elegans: A new model system for the study of learning and memory. Behav Brain Res 37:89-92.
75. Reiner DJ, Newton EM, Tian H, Thomas JH. 1999. Diverse behavioural defects caused by mutations in Caenorhabditis elegans unc-43 CaM kinase II. Nature 402:199-203.
76. Riddle DL, Albert PS. 1997. Genetic and environmental regulation of dauer larva development. In: Riddle DL, Blumenthal T, Meyer BJ, Priess JR, Riddle DL, Blumenthal T, Meyer BJ, Priess JR, editors. C. elegans II. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. p 739-768.
77. Rorth P, Szabo K, Bailey A, Laverty T, Rehm J, Rubin GM, Weigmann K, Milan M, Benes V, Ansorge W, Cohen SM. 1998. Systematic gain-of-function genetics in Drosophila. Development 125:1049-1057.
78. Saeki S, Yamamoto M, Iino Y. 2001. Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J Exp Biol 204:1757-1764.
79. Salkoff L, Butler A, Fawcett G, Kunkel M, McArdle C, Paz-y-Mino G, Nonet M, Walton N, Wang ZW, Yuan A, Wei A. 2001. Evolution tunes the excitability of individual neurons. Neuroscience 103:853-859.
80. Sambongi Y, Nagae T, Liu Y, Yoshimizu T, Takeda K, Wada Y, Futai M. 1999. Sensing of cadmium and copper ions by externally exposed ADL, ASE, and ASH neurons elicits avoidance response in Caenorhabditis elegans. Neuroreport 10:753-757.
81. Satterlee JS, Sasakura H, Kuhara A, Berkeley M, Mori I, Sengupta P. 2001. Specification of thermosensory neuron rate in C. elegans requires ttx-1, a homolog of otd/Otx. Neuron 31:943-956,
82. Sawin ER. 1996. Genetic and Cellular Analysis of Modulated Behaviors in Caenorhabditis elegans. Cambridge, MA: Massachusetts Institute of Technology, Department of biology, p 316.
83. Sawin ER, Ranganathan R, Horvitz HR. 2000, C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26:619-631.
84. Schaffner KF, 1998, Genes, behavior and developmental emergentism: One process, indivisible? Philos Sci 65: 209-252.
85. Sengupta P, Colbert HA, Bargmann CI. 1994. The C. elegans gene odr-7 encodes an olfactory-specific member of the nuclear receptor superfamily. Cell 79:971-980.
86. Simmer F, Tijsterman M, Parrish S, Koushika S, Nonet M, Fire A, Ahringer J, Plasterk R. 2002. Loss of the putative RNA-directed RNA polymerase RRF-3 makes C, elegans hypersensitive to RNAi. Curr Biol 12:1317.
87. Sokolowski MB. 2001. Drosophila: Genetics meets behavior. Nat Rev Genet 2:879-890.
88. Sze JY, Victor M, Loer C, Shi Y, Ruvkun G. 2000. Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403:560-564.
89. Takamori S, Rhee JS, Rosenmund C, Jahn R. 2000. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-194.
90. Tavernarakis N, Wang SL, Dorovkov M, Ryazanov A, Driscoll M. 2000. Heritable and inducible genetic interference by double-stranded RNA encoded by transgenes. Nat Genet 24:180-183.
91. Thomas JH. 1990. Genetic analysis of defecation in Caenorhabditis elegans. Genetics 124:855-872.
92. Tsien JZ. 2000. Linking Hebb's coincidence-detection to memory formation. Curr Opin Neurobiol 10:266-273.
93. Waggoner LE, Zhou GT, Schafer RW, Schafer WR. 1998. Control of alternative behavioral states by serotonin in Caenorhabditis elegans. Neuron 21:203-214.
94. 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 USA 70:817-821.
95. Weinshenker D, Wei A, Salkoff L, Thomas JH. 1999. Block of an ether-a-go-go-like K(+) channel by imipramine rescues egl-2 excitation defects in caenorhabditis elegans. J Neurosci 19:9831-9840.
96. Weiss JB, Suyama KL, Lee HH, Scott MP. 2001. Jelly belly. A Drosophila LDL receptor repeat-containing signal required for mesoderm migration and differentiation, Cell 107:387-398.
97. Wen JY, Kumar N, Morrison G, Rambaldini G, Runciman S, Rousseau J, van der Kooy D. 1997, Mutations that prevent associative learning in C. elegans. Behav Neurosci 111:354-368.
98. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Transact R Soc Lond B [Biol Sci] 314:1-340.
99. Wicks SR, Rankin CH. 1996. The integration of antagonistic reflexes revealed by laser ablation of identified neurons determines habituation kinetics of the Caenorhabditis elegans tap withdrawal response. J Comp Physiol [A] 179:675-685.
100. Wicks SR, Yeh RT, Gish WR, Waterston RH, Plasterk RH. 2001. Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat Genet 28: 160-164.
101. Wittenburg N, Baumeister R. 1999. Thermal avoidance in Caenorhabditis elegans: An approach to the study of nociception. Proc Natl Acad Sci USA 96:10477-10482.
102. Xue D, Tu Y, Chalfie M. 1993. Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science 261:1324-1328.
103. Zheng Y, Brockie PJ, Mellem JE, Madsen DM, Maricq AV. 1999. Neuronal control of locomotion in C. elegans is modified by a dominant mutation in the GLR-1 ionotropic glutamate receptor. Neuron 24:347-361.
104. Zupanc GK. 1996. Peptidergic transmission: From morphological correlates to functional implications. Micron 27: 35-91.