Behavioral plasticity, learning, and memory in C. elegans

Current Opinion in Neurobiology

Volumn 23, Issue 1, 2013, Pages 92-99

  Sasakura, Hiroyuki ^a   Mori, Ikue ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; MEMBRANE PROTEIN; NEUROPEPTIDE Y RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN AHO 3; PROTEIN CASY 1; PROTEIN HEN 1; UNCLASSIFIED DRUG;

AGE 1 GENE; ANIMAL BEHAVIOR; AVERSION; BEHAVIOR; BRAIN FUNCTION; CAENORHABDITIS ELEGANS; CHEMOTAXIS; CRH 1 GENE; EAT 4 GENE; FOOD; GENE; GENE EXPRESSION; HECW 1 GENE; INTERNEURON; LEARNING; LONG TERM MEMORY; MEMORY CONSOLIDATION; MOTONEURON; NEP 2 GENE; NERVE CELL PLASTICITY; NONHUMAN; NPR 1 GENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SMELLING; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; TEMPERATURE; TYRA 3 GENE;

ANIMALS; BRAIN; CAENORHABDITIS ELEGANS; HUMANS; LEARNING; MEMORY; NEURONAL PLASTICITY;

EID: 84872854584     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2012.09.005     Document Type: Review

References (75)

1. Kandel E.R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 2001, 294:1030-1038.
2. Farley J., Alkon D.L. Cellular mechanisms of learning, memory, and information storage. Annu Rev Psychol 1985, 36:419-494.
3. Quinn W.G., Harris W.A., Benzer S. Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci U S A 1974, 71:708-712.
4. Waddell S., Quinn W.G. Flies, genes, and learning. Annu Rev Neurosci 2001, 24:1283-1309.
5. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
6. Burne T., Scott E., van Swinderen B., Hilliard M., Reinhard J., Claudianos C., Eyles D., McGrath J. Big ideas for small brains: what can psychiatry learn from worms, flies, bees and fish?. Mol Psychiatry 2011, 16:7-16.
7. Glanzman D.L. Common mechanisms of synaptic plasticity in vertebrates and invertebrates. Curr Biol 2010, 20:R31-R36.
8. Rand JB, Nonet ML: Synaptic transmission. C. elegans II; 1997: 611-643.
9. Consortium TCeS Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998, 282:2012-2018.
10. Bargmann C.I. Neurobiology of the Caenorhabditis elegans genome. Science 1998, 282:2028-2033.
11. Chalfie M., Jorgensen E.M. C. elegans neuroscience: genetics to genome. Trends Genet 1998, 14:506-512.
12. Bargmann C.I., Kaplan J.M. Signal transduction in the Caenorhabditis elegans nervous system. Annu Rev Neurosci 1998, 21:279-308.
13. Rankin C.H. From gene to identified neuron to behaviour in Caenorhabditis elegans. Nat Rev Genet 2002, 3:622-630.
14. Hobert O. Behavioral plasticity in C. elegans: paradigms, circuits, genes. J Neurobiol 2003, 54:203-223.
15. de Bono M., Maricq A.V. Neuronal substrates of complex behaviors in C. elegans. Annu Rev Neurosci 2005, 28:451-501.
16. Bargmann C.I. Chemosensation in C. elegans. WormBook 2006, 1-29.
17. Giles A.C., Rose J.K., Rankin C.H. Investigations of learning and memory in Caenorhabditis elegans. Int Rev Neurobiol 2006, 69:37-71.
18. Mori I., Sasakura H., Kuhara A. Worm thermotaxis: a model system for analyzing thermosensation and neural plasticity. Curr Opin Neurobiol 2007, 17:712-719.
19. Ardiel E.L., Rankin C.H. An elegant mind: learning and memory in Caenorhabditis elegans. Learn Mem 2012, 17:191-201.
20. Horvitz H.R., Chalfie M., Trent C., Sulston J.E., Evans P.D. Serotonin and octopamine in the nematode Caenorhabditis elegans. Science 1982, 216:1012-1014.
21. Sawin E.R., Ranganathan R., Horvitz H.R. C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 2000, 26:619-631.
22. Kimata T., Sasakura H., Ohnishi N., Nishio N., Mori I. Thermotaxis of C. elegans as a model for temperature perception, neural information processing and neural plasticity. Worm 2012, 1:31-41.
23. Pierce-Shimomura J.T., Faumont S., Gaston M.R., Pearson B.J., Lockery S.R. The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans. Nature 2001, 410:694-698.
24. Hobert O., Johnston R.J., Chang S. Left-right asymmetry in the nervous system: the Caenorhabditis elegans model. Nat Rev Neurosci 2002, 3:629-640.
25. Suzuki H., Thiele T.R., Faumont S., Ezcurra M., Lockery S.R., Schafer W.R. Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature 2008, 454:114-117.
26. Saeki S., Yamamoto M., Iino Y. Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. J Exp Biol 2001, 204:1757-1764.
27. Hukema R.K., Rademakers S., Dekkers M.P., Burghoorn J., Jansen G. Antagonistic sensory cues generate gustatory plasticity in Caenorhabditis elegans. EMBO J 2006, 25:312-322.
28. Hukema R.K., Rademakers S., Jansen G. Gustatory plasticity in C. elegans involves integration of negative cues and NaCl taste mediated by serotonin, dopamine, and glutamate. Learn Mem 2008, 15:829-836.
29. Tomioka M., Adachi T., Suzuki H., Kunitomo H., Schafer W.R., Iino Y. The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 2006, 51:613-625.
30. Ikeda D.D., Duan Y., Matsuki M., Kunitomo H., Hutter H., Hedgecock E.M., Iino Y. CASY-1, an ortholog of calsyntenins/alcadeins, is essential for learning in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2008, 105:5260-5265.
31. Ishihara T., Iino Y., Mohri A., Mori I., Gengyo-Ando K., Mitani S., Katsura I. HEN-1, a secretory protein with an LDL receptor motif, regulates sensory integration and learning in Caenorhabditis elegans. Cell 2002, 109:639-649.
32. Hedgecock E.M., Russell R.L. Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A 1975, 72:4061-4065.
33. Mori I., Ohshima Y. Neural regulation of thermotaxis in Caenorhabditis elegans. Nature 1995, 376:344-348.
34. Mohri A., Kodama E., Kimura K.D., Koike M., Mizuno T., Mori I. Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics 2005, 169:1437-1450.
35. Nishio N., Mohri-Shiomi A., Nishida Y., K-NE N., Kimura K., Kuhara A., Mori I. A novel and conserved protein AHO-3 is required for thermotactic plasticity associated with feeding states in Caenorhabditis elegans. Genes Cells 2012, 17:365-386.
36. Kuhara A., Mori I. Molecular physiology of the neural circuit for calcineurin-dependent associative learning in Caenorhabditis elegans. J Neurosci 2006, 26:9355-9364.
37. Kodama E., Kuhara A., Mohri-Shiomi A., Kimura K.D., Okumura M., Tomioka M., Iino Y., Mori I. Insulin-like signaling and the neural circuit for integrative behavior in C. elegans. Genes Dev 2006, 20:2955-2960.
38. Kimura K.D., Miyawaki A., Matsumoto K., Mori I. The C. elegans thermosensory neuron AFD responds to warming. Curr Biol 2004, 14:1291-1295.
39. Clark D.A., Biron D., Sengupta P., Samuel A.D. The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. J Neurosci 2006, 26:7444-7451.
40. Nishida Y., Sugi T., Nonomura M., Mori I. Identification of the AFD neuron as the site of action of the CREB protein in Caenorhabditis elegans thermotaxis. EMBO Rep 2011, 12:855-862.
41. Biron D., Shibuya M., Gabel C., Wasserman S.M., Clark D.A., Brown A., Sengupta P., Samuel A.D.T. A diacylglycerol kinase modulates long-term thermotactic behavioral plasticity in C. elegans. Nat Neurosci 2006, 9:1499-1505.
42. Ohnishi N., Kuhara A., Nakamura F., Okochi Y., Mori I. Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans. EMBO J 2011, 30:1376-1388.
43. Narayan A., Laurent G., Sternberg P.W. Transfer characteristics of a thermosensory synapse in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2011, 108:9667-9672.
44. Kuhara A., Ohnishi N., Shimowada T., Mori I. Neural coding in a single sensory neuron controlling opposite seeking behaviours in Caenorhabditis elegans. Nat Commun 2011, 2:355.
45. Sugi T., Nishida Y., Mori I. Regulation of behavioral plasticity by systemic temperature signaling in Caenorhabditis elegans. Nat Neurosci 2011, 14:984-992.
46. Pujol N., Link E.M., Liu L.X., Kurz C.L., Alloing G., Tan M.W., Ray K.P., Solari R., Johnson C.D., Ewbank J.J. A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Curr Biol 2001, 11:809-821.
47. Shtonda B.B., Avery L. Dietary choice behavior in Caenorhabditis elegans. J Exp Biol 2006, 209:89-102.
48. Zhang Y., Lu H., Bargmann C.I. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 2005, 438:179-184.
49. Ha H.I., Hendricks M., Shen Y., Gabel C.V., Fang-Yen C., Qin Y., Colon-Ramos D., Shen K., Samuel A.D., Zhang Y. Functional organization of a neural network for aversive olfactory learning in Caenorhabditis elegans. Neuron 2010, 68:1173-1186.
50. Reddy K.C., Andersen E.C., Kruglyak L., Kim D.H. A polymorphism in npr-1 is a behavioral determinant of pathogen susceptibility in C. elegans. Science 2009, 323:382-384.
51. Chang H.C., Paek J., Kim D.H. Natural polymorphisms in C. elegans HECW-1 E3 ligase affect pathogen avoidance behaviour. Nature 2011, 480:525-529.
52. de Bono M., Bargmann C.I. Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 1998, 94:679-689.
53. Gray J.M., Karow D.S., Lu H., Chang A.J., Chang J.S., Ellis R.E., Marletta M.A., Bargmann C.I. Oxygen sensation and social feeding mediated by a C. elegans guanylate cyclase homologue. Nature 2004, 430:317-322.
54. Cheung B.H., Cohen M., Rogers C., Albayram O., de Bono M. Experience-dependent modulation of C. elegans behavior by ambient oxygen. Curr Biol 2005, 15:905-917.
55. Schafer W.R. Egg-laying. WormBook 2005, 1-7.
56. Chase D.L., Koelle M.R. Biogenic Amine Neurotransmitters in C. elegans. WormBook 2007, 1-15.
57. Li C., Kim K. Neuropeptides. WormBook 2008, 1-36.
58. Avery L., You Y.J. C. elegans Feeding. WormBook 2012, 1-23.
59. Alkema M.J., Hunter-Ensor M., Ringstad N., Horvitz H.R. Tyramine functions independently of octopamine in the Caenorhabditis elegans nervous system. Neuron 2005, 46:247-260.
60. Wragg R.T., Hapiak V., Miller S.B., Harris G.P., Gray J., Komuniecki P.R., Komuniecki R.W. Tyramine and octopamine independently inhibit serotonin-stimulated aversive behaviors in Caenorhabditis elegans through two novel amine receptors. J Neurosci 2007, 27:13402-13412.
61. Aston-Jones G., Cohen J.D. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 2005, 28:403-450.
62. Roeder T. Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 2005, 50:447-477.
63. Bendesky A., Tsunozaki M., Rockman M.V., Kruglyak L., Bargmann C.I. Catecholamine receptor polymorphisms affect decision-making in C. elegans. Nature 2011, 472:313-318.
64. Bargmann CI, Mori I: Chemotaxis and Thermotaxis. C. elegans II; 1997: 717-737.
65. Yamada K., Hirotsu T., Matsuki M., Butcher R.A., Tomioka M., Ishihara T., Clardy J., Kunitomo H., Iino Y. Olfactory plasticity is regulated by pheromonal signaling in Caenorhabditis elegans. Science 2010, 329:1647-1650.
66. Morrison G.E., Wen J.Y., Runciman S., van der Kooy D. Olfactory associative learning in Caenorhabditis elegans is impaired in lrn-1 and lrn-2 mutants. Behav Neurosci 1999, 113:358-367.
67. Amano H., Maruyama I.N. Aversive olfactory learning and associative long-term memory in Caenorhabditis elegans. Learn Mem 2011, 18:654-665.
68. Colbert H.A., Bargmann C.I. Odorant-specific adaptation pathways generate olfactory plasticity in C. elegans. Neuron 1995, 14:803-812.
69. Giles A.C., Rankin C.H. Behavioral and genetic characterization of habituation using Caenorhabditis elegans. Neurobiol Learn Mem 2009, 92:139-146.
70. Kimura K.D., Fujita K., Katsura I. Enhancement of odor avoidance regulated by dopamine signaling in Caenorhabditis elegans. J Neurosci 2010, 30:16365-16375.
71. White J.G., Southgate E., Thomson J.N., Brenner S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 1986, 314:1-340.
72. Remy J.J., Hobert O. An interneuronal chemoreceptor required for olfactory imprinting in C. elegans. Science 2005, 309:787-790.
73. Rose J.K., Sangha S., Rai S., Norman K.R., Rankin C.H. Decreased sensory stimulation reduces behavioral responding, retards development, and alters neuronal connectivity in Caenorhabditis elegans. J Neurosci 2005, 25:7159-7168.
74. Timbers T.A., Rankin C.H. Tap withdrawal circuit interneurons require CREB for long-term habituation in Caenorhabditis elegans. Behav Neurosci 2011, 125:560-566.
75. Kauffman A.L., Ashraf J.M., Corces-Zimmerman M.R., Landis J.N., Murphy C.T. Insulin signaling and dietary restriction differentially influence the decline of learning and memory with age. PLoS Biol 2010, 8:e1000372.