A single time-window for protein synthesis-dependent long-term memory formation after one-trial appetitive conditioning

European Journal of Neuroscience

Volumn 21, Issue 5, 2005, Pages 1347-1358

  Fulton, Daniel ^a,b   Kemenes, Ildiko ^a   Andrew, Richard J ^a   Benjamin, Paul R ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anisomycin; Electrophysiology; Long term memory; Lymnaea; Protein

Indexed keywords

ANISOMYCIN;

ANIMAL EXPERIMENT; ARTICLE; CONDITIONING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; LONG TERM MEMORY; LYMNAEA; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RECALL; TRAINING;

ANALYSIS OF VARIANCE; ANIMALS; ANISOMYCIN; APPETITIVE BEHAVIOR; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; DACTINOMYCIN; DOSE-RESPONSE RELATIONSHIP, DRUG; LYMNAEA; MEMORY; NEURAL INHIBITION; PROTEIN SYNTHESIS INHIBITORS; STIMULATION, CHEMICAL; TIME FACTORS;

EID: 17144422425     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2005.03970.x     Document Type: Article

References (49)

1. Alberini, C.M., Ghirardi, M., Metz, R. & Kandel, E.R. (1994) C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell., 76, 1099-1114.
2. Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K. & Watson, J. (1994) Molecular Biology of the Cell, 3rd edn. Garland Publishing, Inc, New York.
3. Alexander, J., Audesirk, T.E. & Audesirk, G.J. (1984) One-trial reward learning in the snail Lymnaea stagnalis. J. Neurobiol., 15, 67-72.
4. Anokhin, K.V. & Rose, S.P. (1991) Learning-induced increase of immediate early gene messenger RNA in the chick forebrain. Eur. J. Neurosci., 2, 162-167.
5. Antonov, I., Antonova, I., Kandel, E. & Hawkins, D. (2001) The contribution of activity-dependent synaptic plasticity to classical conditioning in Aplysia. J. Neurosci., 21, 6413-6422.
6. Antonov, I., Antonova, I., Kandel, E.R. & Hawkins, R.D. (2003) Activity-dependent presynaptic facilitation and hebbian LTP are both required and interact during classical conditioning in Aplysia. Neuron, 37, 135-147.
7. Antonov, I., Kandel, E.R. & Hawkins, R.D. (1999) The contribution of facilitation of monosynaptic PSPs to dishabituation and sensitization of the Aplysia siphon withdrawal reflex. J. Neurosci., 19, 10438-10450.
8. Bailey, C.H., Montarolo, P., Chen, M., Kandel, E.R. & Schacher, S. (1992) Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia. Neuron, 9, 749-758.
9. Balschun, D., Wolfer, D.P., Gass, P., Mantamadiotis, T., Welzl, H., Schutz, G., Frey, J.U. & Lipp, H.P. (2003) Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? J. Neurosci., 23, 6304-6314.
10. Benjamin, P.R. & Elliot, C.J.H. (1989) Snail feeding oscillator. The central pattern generator and its control, by modulatory interneurons. In Jacklet, J. (Ed.), Neuronal and Cellular Oscillators. Marcel Dekker, New York, pp. 173-214.
11. Benjamin, P.R., Staras, K. & Kemenes, G. (2000) A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn. Mem., 7, 124-131.
12. Benjamin, P.R. & Winlow, W. (1981) The distribution of three wide-acting synaptic inputs to identified neurons in the isolated brain of Lymnaea. Comp. Biochem. Physiol. [A], 70, 293-307.
13. Bourtchouladze, R., Abel, T., Berman, N., Gordon, R., Lapidus, K. & Kandel, E.R. (1998) Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn. Mem., 5, 365-374.
14. Castellucci, V.F., Blumenfeld, H., Goelet, P. & Kandel, E.R. (1989) Inhibitor of protein synthesis blocks long-term behavioral sensitization in the isolated gill-withdrawal reflex of Aplysia. J. Neurobiol., 20, 1-9.
15. Crow, T. & Forrester, J. (1990) Inhibition of protein synthesis blocks long-term enhancement of generator potentials produced by one-trial in vivo conditioning in Hermissenda. Proc. Natl Acad. Sci. USA, 87, 4490-4494.
16. Davis, H.P. & Squire, L.R. (1984) Protein synthesis and memory: a review. Psychol. Bull, 96, 518-559.
17. Dezazzo, J.T. & Tully, T. (1995) Dissection of memory formation: from behavioral pharmacology to molecular genetics. Trends Neurosci., 5, 212-218.
18. Epstein, H.T., Child, P.M., Kuzirian, A.M. & 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.
19. Freeman, F.M., Rose, S.P. & Scholey, A.B. (1995) Two time windows of anisomycin-induced amnesia for passive avoidance training in the day-old chick. Neurobiol. Learn. Mem., 63, 291-295.
20. Grecksch, G. & Matthies, H. (1980) Two sensitive periods for the amnesic effect of anisomycin. Pharmacol. Biochem. Behav., 12, 663-665.
21. Grollman, A.P. (1967) Inhibitors of protein biosynthesis. II. Mode of action of anisomycin. J. Biol. Chem., 242, 3226-3233.
22. Guzowski, J.F., Setlow, B., Wagner, E.K. & McGaugh, J.L. (2001) Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci., 21, 5089-5098.
23. Hatakeyama, D., Sadamoto, H. & Ito, E. (2004) 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.
24. Hegde, A.N., Inokuchi, K., Pei, W., Casadio, A., Ghirardi, M., Chain, D.G., Martin, K.C., Kandel, E.R. & Schwartz, J.H. (1997) Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell, 89, 115-126.
25. Huang, Y.Y., Martin, K.C. & Kandel, E.R. (2000) Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J. Neurosci., 20, 6317-6325.
26. Jones, M.W., Errington, M.L., French, P.J., Fine, A., Bliss, T.V., Garel, S., Charnay, P., Bozon, B., Laroche, S. & Davis, S. (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci., 3, 289-296.
27. Jones, N., Kemenes, G. & Benjamin, P.R. (2001) Selective expression of electrical correlates of differential conditioning in a feeding network. J. Neurophysiol., 85, 89-97.
28. Jones, N.G., Kemenes, I., Kemenes, G. & Benjamin, P.R. (2003) A persistent cellular change in a single modulatory neuron contributes to associative long-term memory. Curr. Biol., 13, 1064-1069.
29. Kemenes, I., Kemenes, G., Andrew, R.J., Benjamin, P.R. & 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, G., Staras, K. & Benjamin, P.R. (1997) In vitro classical conditioning of the feeding response in the pond snail Lymnaea stagnalis. J. Neurophysiol., 78, 2351-2362.
31. Kojima, S., Nanakamura, H., Nagayama, S. & 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.
32. Kojima, S.M., Yamanaka, Y., Fujito, Y. & Ito, E. (1996) Differential neuroethological effects of aversive and appetitive reinforcing stimuli on associative learning in Lymnaea stagnalis. Zool. Sci., 13, 803-812.
33. Lamprecht, R. & LeDoux, J. (2004) Structural plasticity and memory. Nat. Neurosci. Rev., 5, 45-54.
34. Montarolo, P.G., Goelet, P., Castellucci, V.F., Morgan, J., Kandel, E.R. & Schacher, S. (1986) A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science, 234, 1249-1254.
35. Ramirez, R.R., Gandhi, C.C., Muzzio, I.A. & Matzel, L.D. (1998) Protein synthesis-dependent memory and neuronal enhancement in Hermissenda are contingent on parameters of training and retention. Learn. Mem., 4, 462-477.
36. Ribeiro, M.J., Serfozo, Z., Papp, A., Kemenes, I., O'Shea, M., Yin, J.C., Benjamin, P.R. & Kemenes, G. (2003) Cyclic AMP response element-binding (CREB)-like proteins in a molluscan brain: cellular localization and learning-induced phosphorylation. Eur. J. Neurosci., 18, 1223-1234.
37. Sangha, S., Scheibenstock, A., McComb, C. & Lukowiak, K. (2003) Intermediate and long-term memories of associative learning are differentially affected by transcription versus translation blockers in Lymnaea. J. Exp. Biol., 206, 1605-1613.
38. Sattelle, D.B. & Lane, N.J. (1972) Architecture of gastropod central nervous tissue in relation to ionic movements. Tissue Cell, 4, 253-270.
39. Schafe, G.E. & LeDoux, J.E. (2000) Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J. Neurosci., 20, RC96.
40. Scharf, M.T., Woo, N.H., Lattal, K.M., Young, J.Z., Nguyen, P.V. & Abel, T. (2002) Protein synthesis is required for the enhancement of long-term potentiation and long-term memory by spaced training. J. Neurophysiol., 87, 2770-2772.
41. Scholey, A.B., Rose, S.P., Zamani, M.R., Bock, E. & Schachner, M. (1993) A role for the neural cell adhesion molecule in a late, consolidating phase of glycoprotein synthesis six hours following passive avoidance training of the young chick. Neuroscience, 55, 499-509.
42. Silva, A.J., Kogan, J.H., Frankland, P.W. & Kida, S. (1998) CREB and memory. Ann. Rev. Neurosci., 21, 127-148.
43. Staras, K., Kemenes, G. & Benjamin, RR. (1998) Neurophysiological correlates of unconditioned and conditioned feeding in the pond snail Lymnaea stagnalis. J. Neurophysiol., 79, 3030-3040.
44. Staras, K., Kemenes, G. & Benjamin, P.R. (1999) Cellular traces of behavioral classical conditioning can be recorded at several specific sites in a simple nervous system. J. Neurosci., 19, 347-357.
45. Sweatt, J.D. (2001) The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J. Neurochem., 76, 1-10.
46. Taubenfeld, S.M., Milekic, M.H., Monti, B. & Alberini, C.M. (2001) .The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta. Nat. Neurosci., 4, 813-818.
47. Tiunova, A.A., Anokhin, K.V. & Rose, S.P. (1998) Two critical periods of protein and glycoprotein synthesis in memory consolidation for visual categorization learning in chicks. Learn. Mem., 4, 401-410.
48. Wustenberg, D., Gerber, B. & Menzel, R. (1998) Short communicaticn: long-but not medium-term retention of olfactory memories in honeybees is impaired by actinomycin D and anisomycin. Eur. J. Neurosci., 10, 2742-2745.
49. Yin, J.-C. & Tully, T. (1996) CREB and the formation of long-term memory. Curr. Opin. Neurobiol., 6, 264-268.