One-trial conditioned taste aversion in Lymnaea: Good and poor performers in long-term memory acquisition

Journal of Experimental Biology

Volumn 210, Issue 7, 2007, Pages 1225-1237

  Sugai, Rio ^a   Azami, Sachiyo ^a   Shiga, Hatsuki ^a   Watanabe, Takayuki ^a   Sadamoto, Hisayo ^b   Kobayashi, Suguru ^b   Hatakeyama, Dai ^a   Fujito, Yutaka ^c   Lukowiak, Ken ^d   Ito, Etsuro ^a,b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^c SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

Cooling; Long term memory; Motivation; One trial conditioning

Indexed keywords

POTASSIUM CHLORIDE; SUCROSE;

ANALYSIS OF VARIANCE; ANIMAL; ARTICLE; COMPARATIVE STUDY; CONDITIONING; FOOD DEPRIVATION; LYMNAEA; MEMORY; PHYSIOLOGY; TASTE; TEMPERATURE;

ANALYSIS OF VARIANCE; ANIMALS; CONDITIONING (PSYCHOLOGY); FOOD DEPRIVATION; LYMNAEA; MEMORY; POTASSIUM CHLORIDE; SUCROSE; TASTE; TEMPERATURE;

GASTROPODA; LYMNAEA; LYMNAEA STAGNALIS; LYMNAEIDAE;

EID: 34248366418     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.02735     Document Type: Article

References (68)

1. Alexander, J., Audesirk, T. E. and Audesirk, G. J. (1984). One-trial reward learning in the snail Lymnaea stagnalis. J. Neurobiol. 15, 67-72.
2. Alkon, D. L., Ikeno, H., Dworkin, J., McPhie, D. L., Olds, J. L., Lederhendler, I., Matzel, L., Schreurs, B. G., Kuzirian, A., Collin, C. et al. (1990). Contraction of neuronal branching volume: an anatomic correlate of Pavlovian conditioning. Proc. Natl. Acad. Sci. USA 87, 1611-1614.
3. Azami, S., Wagatsuma, A., Sadamoto, H., Hatakeyama, D., Usami, T., Fujie, M., Koyanagi, R., Azumi, K., Fujito, Y., Lukowiak, K. et al. (2006). Altered gene activity correlated with long-term memory formation of conditioned taste aversion in Lymnaea. J. Neurosci. Res. 84, 1610-1620.
4. Benjamin, P. R., Staras, K. and Kemenes, G. (2000). A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn. Mem. 7, 124-131.
5. Berman, D. E. and Dudai, Y. (2001). Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science 291, 2417-2419.
6. Bouton, M. E. (1993). Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol. Bull. 114, 80-99.
7. Coutellec, M. A. and Lagadic, L. (2006). Effects of self-fertilization, environmental stress and exposure to xenobiotics on fitness-related traits of the freshwater snail Lymnaea stagnalis. Ecotoxicology 15, 199-213.
8. Davis, H. P. and Squire, L. R. (1984). Protein synthesis and memory: a review. Psychol. Bull. 96, 518-559.
9. Dubnau, J. and Tully, T. (1998). Gene discovery in Drosophila: new insights for learning and memory. Annu. Rev. Neurosci. 21, 407-444.
10. Epstein, H. T., Child, F. M., Kuzirian, A. M. and Alkon, D. L. (2003). Time windows for effects of protein synthesis inhibitors on Pavlovian conditioning in Hermissenda: behavioral aspects. Neurobiol. Learn. Mem. 79, 127-131.
11. Epstein, H. T., Kuzirian, A. M., Child, F. M. and Alkon, D. L. (2004). Two different biological configurations for long-term memory. Neurobiol. Learn. Mem. 81, 12-18.
12. Frenois, F., Le Moine, C. and Cador, M. (2005). The motivational component of withdrawal in opiate addiction: role of associative learning and aversive memory in opiate addiction from a behavioral, anatomical and functional perspective. Rev. Neurosci. 16, 255-276.
13. Fulton, D., Kemenes, I., Andrew, R. J. and Benjamin, P. R. (2005). A single time-window for protein synthesis-dependent long-term memory formation after one-trial appetitive conditioning. Eur. J. Neurosci. 21, 1347-1358.
14. Garcia, J., Kimeldorf, D. J. and Koelling, R. A. (1955). Conditioned aversion to saccharin resulting from exposure to gamma radiation. Science 122, 157-158.
15. Garcia, J., Hankins, W. G. and Rusiniak, K. W. (1974). Behavioral regulation of the melieu interne in man and rat. Science 185, 824-831.
16. Garcia, J., Lasiter, P. S., Bermúdez-Rattoni, F. and Deems, D. A. (1985). A general theory of aversion learning. Ann. NY Acad. Sci. 443, 8-21.
17. Gerber, B., Wustenberg, D., Schutz, A. and Menzel, R. (1998). Temporal determinants of olfactory long-term retention in honeybee classical conditioning: nonmonotonous effects of the conditioning trial interval. Neurobiol. Learn. Mem. 69, 71-78.
18. Hammer, M. and Menzel, R. (1995). Learning and memory in the honeybee. J. Neurosci. 15, 1617-1630.
19. Haney, J. and Lukowiak, K. (2001). Context learning and the effect of context on memory retrieval in Lymnaea. Learn. Mem. 8, 35-43.
20. Hatakeyama, D., Sadamoto, H. and Ito, E. (2004a). Real-time quantitative RT-PCR method for estimation of mRNA level of CCAAT/enhancer binding protein in the central nervous system of Lymnaea stagnalis. Acta Biol. Hung. 55, 157-161.
21. Hatakeyama, D., Fujito, Y., Sakakibara, M. and Ito, E. (2004b). Expression and distribution of transcription factor CCAAT/enhancer-binding protein in the central nervous system of Lymnaea stagnalis. Cell Tissue Res. 318, 631-641.
22. Hatakeyama, D., Sadamoto, H., Watanabe, T., Wagatsuma, A., Kobayashi, S., Fujito, Y., Yamashita, M., Sakakibara, M., Kemenes, G. and Ito, E. (2006). Requirement of new protein synthesis of a transcription factor for memory consolidation: paradoxical changes in mRNA and protein levels of C/EBP. J. Mol. Biol. 356, 569-577.
23. Ito, E., Oka, K., Collin, C., Schreurs, B. G., Sakakibara, M. and Alkon, D. L. (1994). Intracellular calcium signals are enhanced for days after Pavlovian conditioning. J. Neurochem. 62, 1337-1344.
24. Ito, E., Kobayashi, S., Kojima, S., Sadamoto, H. and Hatakeyama, D. (1999). Associative learning in the pond snail, Lymnaea stagnalis. Zool. Sci. 16, 711-723.
25. Kandel, E. R. (2001). The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030-1038.
26. Kandel, E. R. and Squire, L. R. (2000). Neuroscience: breaking down scientific barriers to the study of brain and mind. Science 290, 1113-1120.
27. Kawai, R., Sunada, H., Horikoshi, T. and Sakakibara, M. (2004). Conditioned taste aversion with sucrose and tactile stimuli in the pond snail Lymnaea stagnalis. Neurobiol. Learn. Mem. 82, 164-168.
28. Kemenes, G., Kemenes, I., Michel, M., Papp, A. and Müller, U. (2006). Phase-dependent molecular requirements for memory reconsolidation: differential roles for protein synthesis and protein kinase A activity. J. Neurosci. 26, 6298-6302.
29. Kemenes, I., Kemenes, G., Andrew, R. J., Benjamin, P. R. and O'Shea, M. (2002). Critical time-window for NO-cGMP-dependent long-term memory formation after one-trial appetitive conditioning. J. Neurosci. 22, 1414-1425.
30. Kemenes, I., Straub, V. A., Nikitin, E. S., Staras, K., O'Shea, M., Kemenes, G. and Benjamin, P. R. (2006). Role of delayed nonsynaptic neuronal plasticity in long-term associative memory. Curr. Biol. 16, 1269-1279.
31. Kobayashi, S., Kojima, S., Yamanaka, M., Sadamoto, H., Nakamura, H., Fujito, Y., Kawai, R., Sakakibara, M. and Ito, E. (1998). Operant conditioning of escape behavior in the pond snail, Lymnaea stagnalis. Zool. Sci. 15, 683-690.
32. Kojima, S., Yamanaka, M., Fujito, Y. and Ito, E. (1996). Differential neuroethological effects of aversive and appetitive reinforcing stimuli on associative learning in Lymnaea stagnalis. Zool. Sci. 13, 803-812.
33. Kojima, S., Nakamura, H., Nagayama, S., Fujito, Y. and Ito, E. (1997). Enhancement of an inhibitory input to the feeding central pattern generator in Lymnaea stagnalis during conditioned taste-aversion learning. Neurosci. Lett. 230, 179-182.
34. 2+ signaling in glial cells of snail's brain. Neuroscience 100, 893-900.
35. Kojima, S., Hosono, T., Fujito, Y. and Ito, E. (2001). Optical detection of neuromodulatory effects of conditioned taste aversion in the pond snail Lymnaea stagnalis. J. Neurobiol. 49, 118-128.
36. Lowe, M. R. and Spencer, G. E. (2006). Perturbation of the activity of a single identified neuron affects long-term memory formation in a molluscan semi-intact preparation. J. Exp. Biol. 209, 711-721.
37. Lukowiak, K. (1987). A blood-borne factor from food-satiated Aplysia suppresses the gill withdrawal reflex in in vitro preparations from unsatiated animals. Neurosci. Lett. 77, 205-208.
38. Lukowiak, K. and Freedman, L. (1983). The gill withdrawal reflex is suppressed in sexually active Aplysia. Can. J. Physiol. Pharmacol. 61, 743-748.
39. Lukowiak, K., Sangha, S., McComb, C., Varshney, N., Rosenegger, D., Sadamoto, H. and Scheibenstock, A. (2003). Associative learning and memory in Lymnaea stagnalis: how well do they remember? J. Exp. Biol. 206, 2097-2103.
40. Mackintosh, N. J. (ed.) (1974). Extinction. In The Physiology of Animal Learning, pp. 405-483. London: Academic Press.
41. Margulies, C., Tully, T. and Dubnau, J. (2005). Deconstructing memory in Drosophila. Curr. Biol. 15, R700-R713.
42. Masugi, M., Yokoi, M., Shigemoto, R., Muguruma, K., Watanabe, Y., Sansig, G., van der Putten, H. and Nakanishi, S. (1999). Metabotropic glutamate receptor subtype 7 ablation causes deficit in fear response and conditioned taste aversion. J. Neurosci. 19, 955-963.
43. Matsuo, R., Hitomi, T., Watanabe, S. and Kirino, Y. (2002). Delayed-onset amnesia caused by protein synthesis inhibition in odor-taste associative memory of the terrestrial slug Limax valentianus. Neurosci. Lett. 334, 201-205.
44. McGaugh, J. L. and Izquierdo, I. (2000). The contribution of pharmacology to research on the mechanisms of memory formation. Trends Pharmacol. Sci. 21, 208-210.
45. Milner, B., Squire, L. R. and Kandel, E. R. (1998). Cognitive neuroscience and the study of memory. Neuron 20, 445-468.
46. Mpitsos, G. J. and Collins, S. D. (1975). Learning: rapid aversive conditioning in the gastropod mollusk Pleurobranchaea. Science 188, 954-957.
47. Myers, K. M. and Davis, M. (2002). Behavioral and neural analysis of extinction. Neuron 36, 567-584.
48. Parvez, K., Stewart, O., Sangha, S. and Lukowiak, K. (2005). Boosting intermediate-term into long-term memory. J. Exp. Biol. 208, 1525-1536.
49. Parvez, K., Moisseev, V. and Lukowiak, K. (2006). A context-specific single contingent-reinforcing stimulus boosts intermediate-term memory into long-term memory. Eur. J. Neurosci. 24, 606-616.
50. Rankin, C. H. (2005). Nematode memory: now, where was I? Curr. Biol. 15, R374-R375.
51. Ribeiro, M. J., Schofield, M. G., Kemenes, I., O'Shea, M., Kemenes, G. and Benjamin, P. R. (2005). Activation of MAPK is necessary for long-term memory consolidation following food-reward conditioning. Learn. Mem. 12, 538-545.
52. Rosenegger, D., Roth, S. and Lukowiak, K. (2004). Learning and memory in Lymnaea are negatively altered by acute low-level concentrations of hydrogen sulphide. J. Exp. Biol. 207, 2621-2630.
53. Sadamoto, H., Yamanaka, M., Hatakeyama, D., Nakamura, H., Kojima, S., Yamashita, M. and Ito, E. (2000). Developmental study of anatomical substrate for conditioned taste aversion in Lymnaea stagnalis. Zool. Sci. 17, 141-148.
54. Sadamoto, H., Sato, H., Kobayashi, S., Murakami, J., Aonuma, H., Ando, H., Fujito, Y., Hamano, K., Awaji, M., Lukowiak, K. et al. (2004a). CREB in the pond snail Lymnaea stagnalis. cloning, gene expression and function in identifiable neurons of the central nervous system. J. Neurobiol. 58, 455-466.
55. Sadamoto, H., Azami, S. and Ito, E. (2004b). The expression pattern of CREB genes in the central nervous system of the pond snail Lymnaea stagnalis. Acta Biol. Hung. 55, 163-166.
56. Sakakibara, M. (2006). Comparative study of visuo-vestibular conditioning in Lymnaea stagnalis. Biol. Bull. 210, 298-307.
57. Sakakibara, M., Aritaka, T., Iizuka, A., Suzuki, H., Horikoshi, T. and Lukowiak, K. (2005). Electrophysiological responses to light of neurons in the eye and statocyst of Lymnaea stagnalis. J. Neurophysiol. 93, 493-507.
58. Sangha, S., Scheibenstock, A., Morrow, R. and Lukowiak, K. (2003a). Extinction requires new RNA and protein synthesis and the soma of the cell right pedal dorsal 1 in Lymnaea stagnalis. J. Neurosci. 23, 9842-9851.
59. Sangha, S., Morrow, R., Smyth, K., Cooke, R. and Lukowiak, K. (2003b). Cooling blocks ITM and LTM formation and preserves memory. Neurobiol. Learn. Mem. 80, 130-139.
60. Spencer, G. E., Syed, N. I. and Lukowiak, K. (1999). Neural changes after operant conditioning of the aerial respiratory behavior in Lymnaea stagnalis. J. Neurosci. 19, 1836-1843.
61. Straub, V. A., Styles, B. J., Ireland, J. S., O'Shea, M. and Benjamin, P. R. (2004). Central localization of plasticity involved in appetitive conditioning in Lymnaea. Learn. Mem. 11, 787-793.
62. Sugai, R., Shiga, H., Azami, S., Watanabe, T., Sadamoto, H., Fujito, Y., Lukowiak, K. and Ito, E. (2006). Taste discrimination in conditioned taste aversion of the pond snail Lymnaea stagnalis. J. Exp. Biol. 209, 826-833.
63. ter Maat, A. (1992). Egg laying in the hermaphrodite pond snail Lymnaea stagnalis. Prog. Brain Res. 92, 345-360.
64. Waddell, S. and Quinn, W. G. (2001). Flies, genes, and learning. Annu. Rev. Neurosci. 24, 1283-1309.
65. Wagatsuma, A., Sugai, R., Chono, K., Azami, S., Hatakeyama, D., Sadamoto, H. and Ito, E. (2004). The early snail acquires the learning. Comparison of scores for conditioned taste aversion between morning and afternoon. Acta Biol. Hung. 55, 149-155.
66. Wagatsuma, A., Sadamoto, H., Kitahashi, T., Lukowiak, K., Urano, A. and Ito, E. (2005). Determination of the exact copy numbers of particular mRNAs in a single cell by quantitative real-time RT-PCR. J. Exp. Biol. 208, 2389-2398.
67. Wagatsuma, A., Azami, S., Sakura, M., Hatakeyama, D., Aonuma, H. and Ito, E. (2006). De novo synthesis of CREB in a presynaptic neuron is required for synaptic enhancement involved in memory consolidation. J. Neurosci. Res. 84, 954-960.
68. Yasui, K., Matsuo, R. and Kirino, Y. (2004). Onset of amnesia is delayed with a decrease in inhibition of protein synthesis during odor-taste associative learning in the terrestrial slug Limax valentianus. Zool. Sci. 21, 1163-1166.