Neuronal substrates of complex behaviors in C. elegans

Annual Review of Neuroscience

Volumn 28, Issue , 2005, Pages 451-501

  De Bono, Mario ^a   Maricq, Andres Villu ^b  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

Ca2+ imaging; Caenorhabditis; Foraging; Genetics; Learning; Mating; Neural circuits; Plasticity; Sensory processing; Signal transduction

Indexed keywords

CAENORHABDITIS ELEGANS; CALCIUM SIGNALING; DEFECATION; GENE IDENTIFICATION; GENETIC ANALYSIS; HEAT SENSITIVITY; LOCOMOTION; MATING; NERVE CELL PLASTICITY; NERVOUS SYSTEM; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SMELLING; SOCIAL BEHAVIOR; STATE DEPENDENT LEARNING;

ANIMALS; BEHAVIOR, ANIMAL; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CALCIUM SIGNALING; GENETICS, BEHAVIORAL; LEARNING; LOCOMOTION; MODELS, NEUROLOGICAL; NERVOUS SYSTEM PHYSIOLOGY; NEURONAL PLASTICITY; NEURONS; SEXUAL BEHAVIOR, ANIMAL; SYNAPTIC TRANSMISSION;

EID: 23244432182     PISSN: 0147006X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.neuro.27.070203.144259     Document Type: Review

References (246)

1. Albert PS, Brown SJ, Riddle DL. 1981. Sensory control of dauer larva formation in Caenorhabditis elegans. J. Comp. Neurol. 198:435-51
2. Albertson DG, Thomson JN. 1976. The pharynx of Caenorhabditis elegans. Philos. Trans. R. Soc. London B. Biol. Sci. 275:299-325
3. Anyatonwu GI, Ehrlich BE. 2004. Calcium signaling and polycystin-2. Biochem. Biophys. Res. Commun. 322:1364-73
4. Aronoff R, Mellem JE, Maricq AV, Sprengel R, Seeburg PH. 2004. Neuronal toxicity in Caenorhabditis elegans from an editing site mutant in glutamate receptor channels. J. Neurosci. 24:8135-40
5. Avery L, Horvitz HR. 1990. Effects of starvation and neuroactive drugs on feeding in Caenorhabditis elegans. J. Exp. Zool. 253:263-70
6. Avery L, Thomas JH. 1997. Feeding and defecation. See Riddle et al. 1997, pp. 679-716
7. Bargmann CI. 1998. Neurobiology of the Caenorhabditis elegans genome. Science 282:2028-33
8. Bargmann CI, Avery L. 1995. Laser killing of cells in Caenorhabditis elegans. In Methods in Cell Biology, ed. HF Epstein, DC Shakes, pp. 225-50. New York: Academic
9. Bargmann CI, Hartwieg E, Horvitz HR. 1993. Odorant-selective genes and neurons mediate olfaction in C. elegans. Cell 74:515-27
10. Bargmann CI, Horvitz HR. 1991. Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7:729-42
11. Bargmann CI, Kaplan JM. 1998. Signal transduction in the Caenorhabditis elegans nervous system. Annu. Rev. Neurosci. 21:279-308
12. Bargmann CI, Thomas JH, Horvitz HR. 1990. Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 55:529-38
13. Barr MM, DeModena J, Braun D, Nguyen CQ, Hall DH, Sternberg PW. 2001. The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Curr. Biol. 11:1341-46
14. Barr MM, Sternberg PW. 1999. A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401:386-89
15. Beg AA, Jorgensen EM. 2003. EXP-1 is an excitatory GABA-gated cation channel. Nat. Neurosci. 6:1145-52
16. Bell WJ. 1991. Searching Behavior: The Behavioral Ecology of Finding Resources. New York: Chapman and Hall
17. Bellocchio EE, Reimer RJ, Fremeau RT Jr, Edwards RH. 2000. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289:957-60
18. Berger AJ, Hart AC, Kaplan JM. 1998. G alphas-induced neurodegeneration in Caenorhabditis elegans. J. Neurosci. 18:2871-80
19. Berridge MJ, Bootman MD, Roderick HL. 2003. Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4:517-29
20. Berridge MJ, Lipp P, Bootman MD. 2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1:11-21
21. Bettinger JC, McIntire SL. 2004. State-dependency in C. elegans. Genes Brain Behav. 3:266-72
22. Birnby DA, Link EM, Vowels JJ, Tian H, Colacurcio PL, Thomas JH. 2000. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 155:85-104
23. Branicky R, Shibata Y, Feng J, Hekimi S. 2001. Phenotypic and suppressor analysis of defecation in elk-1 mutants reveals that reaction to changes in temperature is an active process in Caenorhabditis elegans. Genetics 159:997-1006
24. Bredt DS, Nicoll RA. 2003. AMPA receptor trafficking at excitatory synapses. Neuron 40:361-79
25. 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. 21:1510-22
26. 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 31:617-30
27. Burbea M, Dreier L, Dittman JS, Grunwald ME, Kaplan JM. 2002. Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans. Neuron 35:107-20
28. Cassata G, Kagoshima H, Andachi Y, Kohara Y, Durrenberger MB, et al. 2000. The LIM homeobox gene ceh-14 confers thermosensory function to the AFD neurons in Caenorhabditis elegans. Neuron 25:587-97
29. Chalfie M, Sulston JE, White JG, Southgate E, Thomson JN, Brenner S. 1985. The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5:956-64
30. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC. 1994. Green fluorescent protein as a marker for gene expression. Science 263:802-5
31. Chalfie M, White JG. 1988. The nervous system. In The Nematode Caenorhabditis elegans, ed. WB Wood. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
32. Chang S, Johnston RJ Jr, Frokjaer-Jensen C, Lockery S, Hobert O. 2004. MicroRNAs act sequentially and asymmetrically to control chemosensory laterality in the nematode. Nature 430:785-89
33. Chang S, Johnston RJ Jr, Hobert O. 2003. A transcriptional regulatory cascade that controls left/right asymmetry in chemosensory neurons of C. elegans. Genes Dev. 17:2123-37
34. Chao MY, Komatsu H, Fukuto HS, Dionne HM, Hart AC. 2004. Feeding status and serotonin rapidly and reversibly modulate a Caenorhabditis elegans chemosensory circuit. Proc. Natl. Acad. Sci. USA 101:15512-17
35. Chase DL, Pepper JS, Koelle MR. 2004. Mechanism of extrasynaptic dopamine signaling in Caenorhabditis elegans. Nat. Neurosci. 7:1096-103
36. Chasnov JR, Chow KL. 2002. Why are there males in the hermaphroditic species Caenorhabditis elegans? Genetics 160:983-94
37. Cheung BH, Arellano-Carbajal F, Rybicki I, De Bono M. 2004. Soluble guanylate cyclases act in neurons exposed to the body fluid to promote C. elegans aggregation behavior. Curr. Biol. 14:1105-11
38. Coates J, de Bono M. 2002. Antagonistic pathways in neurons exposed to body fluid regulate social feeding in Caenorhabditis elegans. Nature 419:925-29
39. Coburn CM, Bargmann CI. 1996. A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans. Neuron 17:695-706
40. Colbert HA, Bargmann CI. 1995. Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 14:803-12
41. Colbert HA, Bargmann CI. 1997. Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans. Learn. Mem. 4:179-91
42. 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. 17:8259-69
43. Groll NA. 1975. Components and patterns in the behaviour of the nematode Caenorhabditis elegans. J. Zool. London 176:159-76
44. Croll NA, Smith JM. 1978. Integrated behaviour in the feeding phase of Caenorhabditis elegans (Nematoda). J. Zool. London 184:507-17
45. Culotti JG, Russell RL. 1978. Osmotic avoidance defective mutants of the nematode Caenorhabditis elegans. Genetics 90:243-56
46. Dal Santo P, Logan MA, Chisholm AD, Jorgensen EM. 1999. The inositol trisphosphate receptor regulates a 50-second behavioral rhythm in C. elegans. Cell 98:757-67
47. de Bono M, Bargmann CI. 1998. Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94:679-89
48. de Bono M, Tobin D, Davis MW, Avery L, Bargmann C. 2002. Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature 419:899-903
49. Delmas P, Padilla F, Osorio N, Coste B, Raoux M, Crest M. 2004. Polycystins, calcium signaling, and human diseases. Biochem. Biophys. Res. Commun. 322:1374-83
50. Denver DR, Morris K, Thomas WK. 2003. Phylogenetics in Caenorhabditis elegans: an analysis of divergence and outcrossing. Mol. Biol. Evol. 20:393-400
51. Doi M, Iwasaki K. 2002. Regulation of retrograde signaling at neuromuscular junctions by the novel C2 domain protein AEX-1. Neuron 33:249-59
52. Dolmetsch RE, Xu K, Lewis RS. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392:933-36
53. Dreier L, Burbea M, Kaplan JM. 2005. LIN-23-mediated degradation of β-catenin regulates the abundance of GLR-1 glutamate receptors in the ventral nerve cord of C. elegans. Neuron. In press
54. Duerr JS, Frisby DL, Gaskin J, Duke A, Asermely K, et al. 1999. The cat-1 gene of Caenorhabditis elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J. Neurosci. 19:72-84
55. Durbin R. 1987. Studies on the Development and Organisation of the Nervous System of Caenorhabditis elegans. Cambridge, UK: Univ. Cambridge Press
56. Dusenbery DB. 1974. Analysis of chemotaxis in the nematode Caenorhabditis elegansby countercurrent separation. J. Exp. Zool. 188:41-47
57. Dusenbery DB. 1980. Responses of the nematode Caenorhabditis elegans to controlled chemical stimulation. J. Comp. Physiol. 136:327-31
58. Dusenbery DB, Sheridan RE, Russell RL. 1975. Chemotaxis-defective mutants of the nematode Caenorhabditis elegans. Genetics 80:297-309
59. Dwyer ND, Troemel ER, Sengupta P, Bargmann CI. 1998. Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membrane-associated protein. Cell 93:455-66
60. Ehlers MD. 2003. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6:231-42
61. Emmons SW, Lipton J. 2003. Genetic basis of male sexual behavior. J. Neurobiol. 54:93-110
62. Emmons SW, Sternberg PW. 1997. Male development and mating behavior. See Riddle et al. 1997, pp. 295-334
63. Ernstrom GG, Chalfie M. 2002. Genetics of sensory mechanotransduction. Annu. Rev. Genet. 36:411-53
64. 2+ conductances in Caenorhabditis elegans intestinal epithelial cells. J. Gen. Physiol. 122:207-23
65. Fujiwara M, Sengupta P, McIntire SL. 2002. Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36:1091-102
66. Fukuto HS, Ferkey DM, Apicella AJ, Lans H, Sharmeen T, et al. 2004. G protein-coupled receptor kinase function is essential for chemosensation in C. elegans. Neuron 42:581-93
67. Garcia LR, Mehta P, Sternberg PW. 2001. Regulation of distinct muscle behaviors controls the C. elegans male's copulatory spicules during mating. Cell 107:777-88
68. Garcia LR, Sternberg PW. 2003. Caenorhabditis elegans UNC-103 ERG-like potassium channel regulates contractile behaviors of sex muscles in males before and during mating. J. Neurosci. 23:2696-705
69. Ginzburg VE, Roy PJ, Culotti JG. 2002. Semaphorin 1a and semaphorin 1b are required for correct epidermal cell positioning and adhesion during morphogenesis in C. elegans. Development 129:2065-78
70. Gomez M, De Castro E, Guarin E, Sasakura H, Kuhara A, et al. 2001. Ca2+ signaling via the neuronal calcium sensor-1 regulates associative learning and memory in C. elegans. Neuron 30:241-48
71. Goodman MB, Hall DH, Avery L, Lockery SR. 1998. Active currents regulate sensitivity and dynamic range in C. elegans neurons. Neuron 20:763-72
72. Goodman MB, Schwarz EM. 2003. Transducing touch in Caenorhabditis elegans. Annu. Rev. Physiol. 65:429-52
73. Gray JM, Hill JJ, Bargmann CI. 2005. A circuit for navigation in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. In press
74. Gray JM, Karow DS, Lu H, Chang AJ, Chang JS, et al. 2004. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 430:317-22
75. Grunwald ME, Kaplan JM. 2003. Mutations in the ligand-binding and pore domains control exit of glutamate receptors from the endoplasmic reticulum in C. elegans. Neuropharmacology 45:768-76
76. Grunwald ME, Mellem JE, Strutz N, Maricq AV, Kaplan JM. 2004. Clathrin-mediated endocytosis is required for compensatory regulation of GLR-1 glutamate receptors after activity blockade. Proc. Natl. Acad. Sci. USA 101:3190-95
77. Harper JW, Burton JL, Solomon MJ. 2002. The anaphase-promoting complex: It's not just for mitosis anymore. Genes Dev. 16:2179-206
78. Hart AC, Kass J, Shapiro JE, Kaplan JM. 1999. Distinct signaling pathways mediate touch and osmosensory responses in a polymodal sensory neuron. J. Neurosci. 19:1952-58
79. Hart AC, Sims S, Kaplan JM. 1995. Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378:82-85
80. Hedgecock EM, Russell RL. 1975. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 72:4061-65
81. Hilliard MA, Apicella AJ, Kerr R, Suzuki H, Bazzicalupo P, Schafer WR. 2005. In vivo imaging of C. elegans ASH neurons: cellular response and adaptation to chemical repellents. EMBO J. 24:63-72
82. Hilliard MA, Bargmann CI, Bazzicalupo P. 2002. C. elegans responds to chemical repellents by integrating sensory inputs from the head and the tail. Curr. Biol. 12:730-34
83. Hilliard MA, Bergamasco C, Arbucci S, Plasterk RH, Bazzicalupo P. 2004. Worms taste bitter: ASH neurons, QUI-1, GPA-3 and ODR-3 mediate quinine avoidance in Caenorhabditis elegans. EMBO J. 23:1101-11
84. Hills T, Brockie PJ, Maricq AV. 2004. Dopamine and glutamate control area-restricted search behavior in Caenorhabditis elegans. J. Neurosci. 24:1217-25
85. Hirotsu T, Saeki S, Yamamoto M, lino Y. 2000. The Ras-MAPK pathway is important for olfaction in Caenorhabditis elegans. Nature 404:289-93
86. Hobert O, D'Alberti T, Liu Y, Ruvkun G. 1998. Control of neural development and function in a thermoregulatory network by the LIM homeobox gene lin-11. J. Neurosci. 18:2084-96
87. Hobert O, Mori I, Yamashita Y, Honda H, Ohshima Y, et al. 1997. Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19:345-57
88. Hodgkin J. 1983. Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics 103:43-64
89. Hodgkin J, Doniach T. 1997. Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146:149-64
90. Horvitz HR, Chalfie M, Trent C, Sulston JE, Evans PD. 1982. Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 216:1012-14
91. Ishihara T, Iino Y, Mohri A, Mori I, Gengyo-Ando K, et al. 2002. HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans. Cell 109:639-49
92. Iwasaki K, Liu DW, Thomas JH. 1995. Genes that control a temperature-compensated ultra-dian clock in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 92:10317-21
93. Iwasaki K, Staunton J, Saifee O, Nonet M, Thomas JH. 1997. aex-3 encodes a novel regulator of presynaptic activity in C. elegans. Neuron 18:613-22
94. Iwasaki K, Toyonaga R. 2000. The Rab3 GDP/GTP exchange factor homolog AEX-3 has a dual function in synaptic transmission. EMBO J. 19:4806-16
95. Jansen G, Thijssen KL, Werner P, van der Horst M, Hazendonk E, Plasterk RH. 1999. The complete family of genes encoding G proteins of Caenorhabditis elegans. Nat. Genet. 21:414-19
96. 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. 21:986-94
97. Jee C, Lee J, Lee JI, Lee WH, Park BJ, et al. 2004. SHN-1, a Shank homologue in C. elegans, affects defecation rhythm via the inositol-1,4,5- trisphosphate receptor. FEBS Lett. 561:29-36
98. Johnston RJ, Hobert O. 2003. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426:845-49
99. Juo P, Kaplan JM. 2004. The anaphase-promoting complex regulates the abundance of GLR-1 glutamate receptors in the ventral nerve cord of C. elegans. Curr. Biol. 14:2057-62
100. Kahn-Kirby AH, Dantzker JL, Apicella AJ, Schafer WR, Browse J, et al. 2004. Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo. Cell 119:889-900
101. Kaletta T, Van der Craen M, Van Geel A, Dewulf N, Bogaert T, et al. 2003. Towards understanding the polycystins. Nephron. Exp. Nephrol. 93:e9-17
102. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. 2003. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421:231-37
103. Kaplan JM, Horvitz HR. 1993. A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 90:2227-31
104. Kass J, Jacob TC, Kim P, Kaplan JM. 2001. The EGL-3 proprotein convertase regulates mechanosensory responses of Caenorhabditis elegans. J. Neurosci. 21:9265-72
105. Kellenberger S, Schild L. 2002. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 82:735-67
106. Kennedy S, Wang D, Ruvkun G. 2004. A conserved siRNA-degrading RNase negatively regulates RNA interference in C. elegans. Nature 427:645-49
107. 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 26:583-94
108. Kim E, Sheng M. 2004. PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5:771-81
109. Kim K, Li C. 2004. Expression and regulation of an FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. J. Comp. Neurol. 475:540-50
110. Kimura KD, Miyawaki A, Matsumoto K, Mori I. 2004. The C. elegans thermosensory neuron AFD responds to warming. Curr. Biol. 14:1291-95
111. Kippert F, Saunders DS, Blaxter ML. 2002. Caenorhabditis elegans has a circadian clock. Curr. Biol. 12:R47-49
112. Koesling D. 1999. Studying the structure and regulation of soluble guanylyl cyclase. Methods 19:485-93
113. Komatsu H, Jin YH, L'Etoile N, Mori I, Bargmann CI, et al. 1999. Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of Caenorhabditis elegans in cultured cells. Brain Res. 821:160-68
114. Komatsu H, Mori I, Rhee JS, Akaike N, Ohshima Y. 1996. Mutations in a cyclic nucleotidegated channel lead to abnormal thermosensation and chemosensation in C. elegans. Neuron 17:707-18
115. Kubiak TM, Larsen MJ, Nulf SC, Zantello MR, Burton KJ, et al. 2003. Differential activation of "social" and "solitary" variants of the Caenorhabditis elegans G protein-coupled receptor NPR-1 by its cognate ligand AF9. J. Biol. Chem. 278:33724-29
116. 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 33:751-63
117. L'Etoile ND, Bargmann CI. 2000. Olfaction and odor discrimination are mediated by the C. elegans guanylyl cyclase ODR-1. Neuron 25:575-86
118. L'Etoile ND, Coburn CM, Eastham J, Kistler A, Gallegos G, Bargmann CI. 2002. The cyclic GMP-dependent protein kinase EGL-4 regulates olfactory adaptation in C. elegans. Neuron 36:1079-89
119. Lackner MR, Nurrish SJ, Kaplan JM. 1999. Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24:335-46
120. Lans H, Rademakers S, Jansen G. 2004. A network of stimulatory and inhibitory Galpha-subunits regulates olfaction in Caenorhabditis elegans. Genetics 167:1677-87
121. Law E, Nuttley WM, van der Kooy D. 2004. Contextual taste cues modulate olfactory learning in C. elegans by an occasion-setting mechanism. Curr. Biol. 14:1303-8
122. Lee HH, Norris A, Weiss JB, Frasch M. 2003. Jelly belly protein activates the receptor tyrosine kinase Alk to specify visceral muscle pioneers. Nature 425:507-12
123. 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. 19:159-67
124. Li C, Kim K, Nelson LS. 1999a. FMRFamide-related neuropeptide gene family in Caenorhabditis elegans. Brain Res. 848:26-34
125. Li C, Nelson L, Kim K, Nathoo A, Hart AC. 1999b. Neuropeptide gene families in the nematode Caenorhabditis elegans. Ann. N.Y. Acad. Sci. 897:239-52
126. Li J, Zhu X, Boston R, Ashton FT, Gamble HR, Schad GA. 2000. Thermotaxis and thermosensory neurons in infective larvae of Haemonchus contortus, a passively ingested nematode parasite. J. Comp. Neurol. 424:58-73
127. Liedtke W, Tobin DM, Bargmann CI, Friedman JM. 2003. Mammalian TRPV4 (VR-OAC) directs behavioral responses to osmotic and mechanical stimuli in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 100(Suppl. 2):14531-36
128. Lints R, Jia L, Kim K, Li C, Emmons SW. 2004. Axial patterning of C. elegans male sensilla identities by selector genes. Dev. Biol. 269:137-51
129. Lipton J, Kleemann G, Ghosh R, Lints R, Emmons SW. 2004. Mate searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. J. Neurosci. 24:7427-34
130. Liu DW, Thomas JH. 1994. Regulation of a periodic motor program in C. elegans. J. Neurosci. 14:1953-62
131. Liu KS, Sternberg PW. 1995. Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14:79-89
132. Loer CM, Kenyon CJ. 1993. Serotonin-deficient mutants and male mating behavior in the nematode Caenorhabditis elegans. J. Neurosci. 13:5407-17
133. Lopez PM, Boston R, Ashton FT, Schad GA. 2000. The neurons of class ALD mediate thermotaxis in the parasitic nematode, Strongyloides stercoralis. Int. J. Parasitol. 30:1115-21
134. Malenka RC, Bear MF. 2004. LTP and LTD: an embarrassment of riches. Neuron 44:5-21
135. 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
136. Martin TF. 2002. Prime movers of synaptic vesicle exocytosis. Neuron 34:9-12
137. Mathews EA, Garcia E, Santi CM, Mullen GP, Thacker C, et al. 2003. Critical residues of the Caenorhabditis elegans unc-2 voltage-gated calcium channel that affect behavioral and physiological properties. J. Neurosci. 23:6537-45
138. McIntire SL, Jorgensen E, Horvitz HR. 1993a. Genes required for GABA function in Caenorhabditis elegans. Nature 364:334-37
139. McIntire SL, Jorgensen E, Kaplan J, Horvitz HR. 1993b. The GABAergic nervous system of Caenorhabditis elegans. Nature 364:337-41
140. Mee CJ, Tomlinson SR, Perestenko PV, De Pomerai D, Duce IR, et al. 2004. Latrophilin is required for toxicity of black widow spider venom in Caenorhabditis elegans. Biochem. J. 378:185-91
141. Mellem JE, Brockie PJ, Zheng Y, Madsen DM, Maricq AV. 2002. Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. elegans. Neuron 36:933-44
142. Miller KG, Emerson MD, Rand JB. 1999. Goalpha and diacylglycerol kinase negatively regulate the Gqalpha pathway in C. elegans. Neuron 24:323-33
143. Montell C. 1999. Visual transduction in Drosophila. Annu. Rev. Cell Dev. Biol. 15:231-68
144. Mori I. 1999. Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. Annu. Rev. Genet. 33:399-422
145. Mori I, Ohshima Y. 1995. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 376:344-48
146. 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. 115:640-49
147. 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. 113:358-67
148. Morton DB. 2005. Atypical soluble guanylate cyclases in Drosophila can function as molecular oxygen sensors. J. Biol. Chem. In press
149. Morton DB, Hudson ML, Waters E, O'Shea M. 1999. Soluble guanylyl cyclases in Caenorhabditis elegans: NO is not the answer. Curr. Biol. 9:R546-47
150. Nass R, Blakely RD. 2003. The Caenorhabditis elegans dopaminergic system: opportunities for insights into dopamine transport and neurodegeneration. Annu. Rev. Pharmacol. Toxicol. 43:521-44
151. Nauli SM, Zhou J. 2004. Polycystins and mechanosensation in renal and nodal cilia. Bioessays 26:844-56
152. Niebur E, Erdos P. 1993. Theory of the locomotion of nematodes: control of the somatic motor neurons by interneurons. Math Biosci. 118:51-82
153. Nolan KM, Sarafi-Reinach TR, Horne JG, Saffer AM, Sengupta P. 2002. The DAF-7 TGF-beta signaling pathway regulates chemosensory receptor gene expression in C. elegans. Genes Dev. 16:3061-73
154. Nonet ML. 1999. Visualization of synaptic specializations in live C. elegans with synaptic vesicle protein-GFP fusions. J. Nettrosci. Methods 89:33-40
155. Nonet ML, Grundahl K, Meyer BJ, Rand JB. 1993. Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73:1291-305
156. Nonet ML, Holgado AM, Brewer F, Serpe CJ, Norbeck BA, et al. 1999. UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol. Biol. Cell. 10:2343-60
157. Nonet ML, Staunton JE, Kilgard MP, Fergestad T, Hartwieg E, et al. 1997. Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J. Neurosci. 17:8061-73
158. Nurrish S, Segalat L, Kaplan JM. 1999. Serotonin inhibition of synaptic transmission: Galpha(O) decreases the abundance of UNC-13 at release sites. Neuron 24:231-42
159. Nuttley WM, Atkinson-Leadbeater KP, Van Der Kooy D. 2002. Serotonin mediates food-odor associative learning in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 99:12449-54
160. O'Hagan R, Chalfie M, Goodman MB. 2005. The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat. Neurosci. 8:43-50
161. Peckol EL, Troemel ER, Bargmann CI. 2001. Sensory experience and sensory activity regulate chemosensory receptor gene expression in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98:11032-38
162. Perkins LA, Hedgecock EM, Thomson JN, Culotti JG. 1986. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117:456-87
163. Peters JM. 2002. The anaphase-promoting complex: proteolysis in mitosis and beyond. Mol. Cell 9:931-43
164. 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 410:694-98
165. Pierce-Shimomura JT, Morse TM, Lockery SR. 1999. The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J. Neurosci. 19:9557-69
166. Raizen DM, Avery L. 1994. Electrical activity and behavior in the pharynx of Caenorhabditis elegans. Neuron 12:483-95
167. Rand JB, Nonet ML. 1997. Neurotransmitter assignments for specific neurons. See Riddle etal. 1997, pp. 1049-52
168. Ranganathan R, Cannon SC, Horvitz HR. 2000. MOD-1 is a serotonin-gated chloride channel that modulates locomotory behaviour in C. elegans. Nature 408:470-75
169. 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. 21:5871-84
170. Rankin CH. 2000. Context conditioning in habituation in the nematode Caenorhabditis elegans. Behav. Neurosci. 114:496-505
171. 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. 20:4337-44
172. 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
173. Ren P, Lim CS, Johnsen R, Albert PS, Pilgrim D, Riddle DL. 1996. Control of C. elegans larval development by neuronal expression of a TGF-β homolog. Science 274:1389-91
174. Richmond JE, Davis WS, Jorgensen EM. 1999. UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat. Neurosci. 2:959-64
175. Riddle DL, Blumenthal T, Meyer BJ, Priess JR, eds. 1997. C. elegans II. Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
176. Roayaie K, Crump JG, Sagasti A, Bargmann CI. 1998. The G alpha protein ODR-3 mediates olfactory and nociceptive function and controls cilium morphogenesis in C. elegans olfactory neurons. Neuron 20:55-67
177. Robertson HM. 2001. Updating the str and srj (stl) families of chemoreceptors in Caenorhabditis nematodes reveals frequent gene movement within and between chromosomes. Chem. Senses 26:151-59
178. Rogers C, Reale V, Kim K, Chatwin H, Li C, et al. 2003. Inhibition of Caenorhabditis elegans social feeding by FMRFamide-related peptide activation of NPR-1. Nat. Neurosci. 6:1178-85
179. Rongo C, Kaplan JM. 1999. CaMKII regulates the density of central glutamatergic synapses in vivo. Nature 402:195-99
180. Rongo C, Whitfield CW, Rodal A, Kim SK, Kaplan JM. 1998. LIN-10 is a shared component of the polarized protein localization pathways in neurons and epithelia. Cell 94:751-59
181. Rose JK, Kaun KR, Chen SH, Rankin CH. 2003. GLR-1, a non-NMDA glutamate receptor homolog, is critical for long-term memory in Caenorhabditis elegans. J. Neurosci. 23:9595-99
182. Rose JK, Kaun KR, Rankin CH. 2002. A new group-training procedure for habituation demonstrates that presynaptic glutamate release contributes to long-term memory in Caenorhabditis elegans. Learn. Mem. 9:130-37
183. Ryu WS, Samuel AD. 2002. Thermotaxis in Caenorhabditis elegans analyzed by measuring responses to defined Thermal stimuli. J. Neurosci. 22:5727-33
184. 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. 204:1757-64
185. Saigusa T, Ishizaki S, Watabiki S, Ishii N, Tanakadate A, et al. 2002. Circadian behavioural rhythm in Caenorhabditis elegans. Curr. Biol. 12:R46-47
186. Sambongi Y, Nagae T, Liu Y, Yoshimizu T, Takeda K, et al. 1999. Sensing of cadmium and copper ions by externally exposed ADL, ASE, and ASH neurons elicits avoidance response in Caenorhabditis elegans. Neuroreport 10:753-57
187. Sambongi Y, Takeda K, Wakabayashi T, Ueda I, Wada Y, Futai M. 2000. Caenorhabditis elegans senses protons through amphid chemosensory neurons: proton signals elicit avoidance behavior. Neuroreport 11:2229-32
188. Samuel AD, Silva RA, Murthy VN. 2003. Synaptic activity of the AFD neuron in Caenorhabditis elegans correlates with thermotactic memory. J. Neurosci. 23:373-76
189. Sanyal S, Wintle RF, Kindt KS, Nuttley WM, Arvan R, et al. 2004. Dopamine modulates the plasticity of mechanosensory responses in Caenorhabditis elegans. EMBO J. 23:473-82
190. Satterlee JS, Ryu WS, Sengupta P. 2004. The CMK-1 CaMKI and the TAX-4 cyclic nucleotide-gated channel regulate thermosensory neuron gene expression and function in C. elegans. Curr. Biol. 14:62-68
191. Satterlee JS, Sasakura H, Kuhara A, Berkeley M, Mori I, Sengupta P. 2001. Specification of thermosensory neuron fate in C. elegans requires ttx-1, a homolog of otd/Otx. Neuron 31:943-56
192. 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 26:619-31
193. Schackwitz WS, Inoue T, Thomas JH. 1996. Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 17:719-28
194. Schafer WR, Kenyon CJ. 1995. A calcium-channel homologue required for adaptation to dopamine and serotonin in Caenorhabditis elegans. Nature 375:73-78
195. Schuster S, Marhl M, Hofer T. 2002. Modelling of simple and complex calcium oscillations. From single-cell responses to intercellular signalling. Eur. J. Biochem. 269:1333-55
196. Segalat L, Elkes DA, Kaplan JM. 1995. Modulation of serotonin-controlled behaviors by Go in Caenorhabditis elegans. Science 267:1648-51
197. Seidenman KJ, Steinberg JP, Huganir R, Malinow R. 2003. Glutamate receptor subunit 2 Serine 880 phosphorylation modulates synaptic transmission and mediates plasticity in CA1 pyramidal cells. J. Neurosci. 23:9220-28
198. Sengupta P, Chou JH, Bargmann CI. 1996. odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84:899-909
199. Sheng M, Kim E. 2000. The Shank family of scaffold proteins. J. Cell. Sci. 113(Pt. 11):1851-56
200. Shim J, Umemura T, Nothstein E, Rongo C. 2004. The unfolded protein response regulates glutamate receptor export from the endoplasmic reticulum. Mol. Biol. Cell. 15:4818-28
201. Shingai R. 2000. Durations and frequencies of free locomotion in wild type and GABAergic mutants of Caenorhabditis elegans. Neurosci. Res. 38:71-83
202. Simon JM, Sternberg PW. 2002. Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 99:1598-603
203. Sulston JE, Albertson DG, Thomson JN. 1980. The Caenorhabditis elegans male: postembryonic development of nongonadal structures. Dev. Biol. 78:542-76
204. Sulston JE, Horvitz HR. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56:110-56
205. Sulston JE, Schierenberg E, White JG, Thomson JN. 1983. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100:64-119
206. Sulston JE, White JG. 1980. Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. Dev. Biol. 78:577-97
207. Sze JY, Ruvkun G. 2003. Activity of the Caenorhabditis elegans UNC-86 POU transcription factor modulates olfactory sensitivity. Proc. Natl. Acad. Sci. USA 100:9560-65
208. Takamori S, Rhee JS, Rosenmund C, Jahn R. 2000. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407:189-94
209. Take-Uchi M, Kawakami M, Ishihara T, Amano T, Kondo K, Katsura I. 1998. An ion channel of the degenerin/epithelial sodium channel superfamily controls the defecation rhythm in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 95:11775-80
210. Tavernarakis N, Shreffler W, Wang S, Driscoll M. 1997. unc-8, a DEG/ENaC family member, encodes a subunit of a candidate mechanically gated channel that modulates C. elegans locomotion. Neuron 18:107-19
211. 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. 24:180-83
212. Thacker C, Rose AM. 2000. A look at the Caenorhabditis elegans Kex2/Subtilisin-like proprotein convertase family. Bioessays 22:545-53
213. Thomas JH. 1990. Genetic analysis of defecation in Caenorhabditis elegans. Genetics 124:855-72
214. Thomas JH, Birnby DA, Vowels JJ. 1993. Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans. Genetics 134:1105-17
215. Tobin D, Madsen D, Kahn-Kirby A, Peckol E, Moulder G, et al. 2002. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35:307-18
216. Troemel ER. 1999. Chemosensory Receptors in Caenorhabditis Elegans. Ph.D. Thesis, Univ. Calif. San Francisco
217. Troemel ER, Chou JH, Dwyer ND, Colbert HA, Bargmann CI. 1995. Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83:207-18
218. Troemel ER, Kimmel BE, Bargmann CI. 1997. Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans. Cell 91:161-69
219. 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 99:3 87-98
220. Tsalik EL, Hobert O. 2003. Functional mapping of neurons that control locomotory behavior in Caenorhabditis elegans. J. Neurobiol. 56:178-97
221. Turrigiano GG, Nelson SB. 2004. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5:97-107
222. Vowels JJ, Thomas JH. 1994. Multiple chemosensory defects in daf-11 and daf-21 mutants of Caenorhabditis elegans. Genetics 138:303-16
223. Wakabayashi T, Kitagawa I, Shingai R. 2004. Neurons regulating the duration of forward locomotion in Caenorhabditis elegans. Neurosci. Res. 50:103-11
224. Walker DS, Gower NJ, Ly S, Bradley GL, Baylis HA. 2002a. Regulated disruption of inositol 1,4,5-trisphosphate signaling in Caenorhabditis elegans reveals new functions in feeding and embryogenesis. Mol. Biol. Cell. 13:1329-37
225. Walker DS, Ly S, Gower NJ, Baylis HA. 2004. IRI-1, a LIN-15B homologue, interacts with inositol-1,4,5-triphosphate receptors and regulates gonadogenesis, defecation, and pharyngeal pumping in Caenorhabditis elegans. Mol. Biol. Cell. 15:3073-82
226. Walker DS, Ly S, Lockwood KC, Baylis HA. 2002b. A direct interaction between IP(3) receptors and myosin II regulates IP(3) signaling in C. elegans. Curr. Biol. 12:951-56
227. 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 70:817-21
228. Ward S, Thomson N, White JG, Brenner S. 1975. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurol. 160:313-37
229. Ware RW, Clark D, Crossland K, Russell RL. 1975. The nerve ring of the nematode Caenorhabditis elegans: sensory input and motor output. J. Comp. Neurol. 162:71-110
230. Weinshenker D, Wei A, Salkoff L, Thomas JH. 1999. Block of an ether-a-go-go-tike K(+) channel by imipramine rescues egl-2 excitation defects in Caenorhabditis elegans. J. Neurosci. 19:9831-40
231. 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 107:387-98
232. Wen JY, Kumar N, Morrison G, Rambaldini G, Runciman S, et al. 1997. Mutations that prevent associative learning in C. elegans. Behav. Neurosci. 111:354-68
233. Wes PD, Bargmann CI. 2001. C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature 410:698-701
234. White JG, Southgate E, Thomson JN, Brenner S. 1986. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. Roy. Soc. (London) B 314:1-340
235. Wicks SR, Rankin CH. 1995. Integration of mechanosensory stimuli in Caenorhabditis elegans. J. Neurosci. 15:2434-44
236. Wittenburg N, Baumeister R. 1999. Thermal avoidance in Caenorhabditis elegans: an approach to the study of nociception. Proc. Natl. Acad. Sci. USA 96:10477-82
237. Wong A, Boutis P, Hekimi S. 1995. Mutations in the clk-1 gene of Caenorhabditis elegans affect developmental and behavioral timing. Genetics 139:1247-59
238. Yin X, Gower NJ, Baylis HA, Strange K. 2004. Inositol 1,4,5-trisphosphate signaling regulates rhythmic contractile activity of myoepithelial sheath cells in Caenorhabditis elegans. Mol. Biol. Cell. 15:3938-49
239. Yoda A, Sawa H, Okano H. 2000. MSI-1, a neural RNA-binding protein, is involved in male mating behaviour in Caenorhabditis elegans. Genes Cells 5:885-95
240. Yu H, Pretot RF, Burglin TR, Sternberg PW. 2003. Distinct roles of transcription factors EGL-46 and DAF-19 in specifying the functionality of a polycystin-expressing sensory neuron necessary for C. elegans male vulva location behavior. Development 130:5217-27
241. 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. USA 94:3384-87
242. Zariwala HA, Miller AC, Faumont S, Lockery SR. 2003. Step response analysis of thermotaxis in Caenorhabditis elegans. J. Neurosci. 23:4369-77
243. 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 24:347-61
244. Zheng Y, Mellem JE, Brockie PJ, Madsen DM, Maricq AV. 2004. SOL-1 is a CUB-domain protein required for GLR-1 glutamate receptor function in C. elegans. Nature 427:451-57
245. Zuo J, De Jager PL, Takahashi KA, Jiang W, Linden DJ, Heintz N. 1997. Neurodegeneration in Lurcher mice caused by mutation in delta2 glutamate receptor gene. Nature 388:769-73
246. Zwaal RR, Broeks A, van Meurs J, Groenen JT, Plasterk RH. 1993. Target-selected gene inactivation in Caenorhabditis elegans by using a frozen transposon insertion mutant bank. Proc. Natl. Acad. Sci. USA 90:7431-35