Intrahippocampal infusions of anisomycin produce amnesia: Contribution of increased release of norepinephrine, dopamine, and acetylcholine

Learning and Memory

Volumn 16, Issue 5, 2009, Pages 308-314

  Qi, Zhenghan ^a   Gold, Paul E ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ANISOMYCIN; DOPAMINE; NORADRENALIN; PROPRANOLOL; SEROTONIN;

ACETYLCHOLINE RELEASE; AMNESIA; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; DOPAMINE RELEASE; HIPPOCAMPUS; HISTOLOGY; LATENT PERIOD; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MICRODIALYSIS; NEUROTRANSMITTER RELEASE; NONHUMAN; NORADRENALIN RELEASE; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RAT; TRAINING;

ACETYLCHOLINE; AMNESIA; ANIMALS; ANISOMYCIN; DOPAMINE; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; MEMORY; MICRODIALYSIS; NEUROTRANSMITTER AGENTS; NOREPINEPHRINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SYNTHESIS INHIBITORS; RATS;

EID: 66149130703     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.1333409     Document Type: Article

References (74)

1. Abraham, W.C. and WIlliams, J.M. 2008. LTP maintenance and its protein synthesis dependence. Neurobiol. Learn. Mem. 89: 260-268.
2. Agnihotri, N.T., Hawkins, R.D., Kandel, E.R., and Kentros, C. 2004. The long-term stability of new hippocampal place fields requires new protein synthesis. Proc. Natl. Acad. Sci. 101: 3656-3661. (Pubitemid 38338250)
3. Akirav, I. and Maroun, M. 2006. Ventromedial prefrontal cortex is obligatory for consolidation and reconsolidation of object recognition memory. Cereb. Cortex 16: 1759-1765.
4. Alberini, C.M. 2008. The role of protein synthesis during the labile phases of memory: Revisiting the skepticism. Neurobiol. Learn. Mem. 89: 234-246.
5. Arnsten, A.F.T., Ramos, B.P., Birnbaum, S.G., and Taylor, J.R. 2005. Protein kinase A as a therapeutic target for memory disorders: Rationale and challenges. Trends Mol. Med. 11: 121-128. (Pubitemid 40348989)
6. Artinian, J., De Jaeger, X., Fellini, L., de Saint Blanquat, P., and Roullet, P. 2007. Reactivation with a simple exposure to the experimental environment is sufficient to induce reconsolidation requiring protein synthesis in the hippocampal CA3 region in mice. Hippocampus 17: 181-191. (Pubitemid 46427672)
7. Barraco, R.A. and Stettner, L.J. 1976. Antibiotics and memory. Psychol. Bull. 83: 242-302.
8. Barriantos, R.M., O'Reilly, R.C., and Rudy, J.W. 2002. Memory for context is impaired by injecting anisomycin into dorsal hippocampus following context exploration. Behav. Brain Res. 134: 299-306.
9. Bourtchouladze, R., Abel, T., Berman, N., Gordon, R., Lapidus, K., and 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. (Pubitemid 29115266)
10. Canal, C.E. and Gold, P.E. 2007. Different temporal profiles of amnesia after intrahippocampus and intra-amygdala infusions of anisomycin. Behav. Neurosci. 121: 732-741. (Pubitemid 47454587)
11. Canal, C.E., Chang, Q., and Gold, P.E. 2007. Amnesia produced by altered release of neurotransmitters after intra-amygdala injections of a protein synthesis inhibitor. Proc. Natl. Acad. Sci. 104: 12500-12505. (Pubitemid 47206167)
12. Canal, C.E., Chang, Q., and Gold, P.E. 2008. Intra-amygdala injections of CREB antisense impair inhibitory avoidance memory: Role of norepinephrine and acetylcholine. Learn. Mem. 15: 677-686.
13. Chang, Q., Savage, L.M., and Gold, P.E. 2006. Microdialysis measures of functional increases in ACh release in the hippocampus with and without inclusion of acetylcholinesterase inhibitors in the perfusate. J. Neurochem. 97: 697-706.
14. Clayton, D.F. 2000. The genomic action potential. Neurobiol. Learn. Mem. 74: 185-216.
15. Davis, S. and Laroche, S. 2006. Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: A review. Genes Brain Behav. (Suppl. 2) 5: 61-72.
16. Davis, H.P. and Squire, L.R. 1984. Protein synthesis and memory: A review. Psychol. Bull. 96: 518-559.
17. Debiec, J., LeDoux, J.E., and Nader, K. 2002. Cellular and systems reconsolidation in the hippocampus. Neuron 36: 527-538. (Pubitemid 35291098)
18. Dudai, Y. 2002. Molecular bases of long-term memories: A question of persistence. Curr. Opin. Neurobiol. 12: 211-216. (Pubitemid 34518342)
19. Duvarci, S., Nader, K., and LeDoux, J.E. 2005. Activation of extracellular signal-regulated kinase- mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning. Eur. J. Neurosci. 21: 283-289. (Pubitemid 40193898)
20. Edwards, D.R. and Mahadevan, L.C. 1992. Protein synthesis inhibitors differentially superinduce c-fos and c-jun by three distinct mechanisms: Lack of evidence for labile repressors. EMBO J. 11: 2415-2424.
21. Flexner, L.B. and Goodman, R.H. 1975. Studies on memory: Inhibitors of protein synthesis also inhibit catecholamine synthesis. Proc. Natl. Acad. Sci. 72: 4660-4663.
22. Flood, J.F., Bennett, E.L., Orme, A.E., and Rosenzweig, M.R. 1975. Effects of protein synthesis inhibition on memory for active avoidance training. Physiol. Behav. 14: 177-184.
23. Flood, J.F., Bennett, E.L., Orme, A.E., Rosenzweig, M.R., and Jarvik, M.E. 1978. Memory: Modification of anisomycin-induced amnesia by stimulants and depressants. Science 199: 324-326. (Pubitemid 8298027)
24. Fonseca, R., Nagerl, U.V., and Bonhoeffer, T. 2006a. Neuronal activity determines the protein synthesis dependence of long-term potentiation. Nat. Neurosci. 9: 478-480.
25. Fonseca, R., Vabulas, R.M., Hartl, F.U., Bonhoeffer, T., and Nagerl, U.V. 2006b. A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 52: 239-245. (Pubitemid 44548341)
26. Frey, U. and Morris, R.G. 1998. Synaptic tagging: Implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci. 21: 181-188. (Pubitemid 28191809)
27. Gold, P.E. 2006. The many faces of amnesia. Learn. Mem. 13: 506-514. (Pubitemid 44500633)
28. Gold, P.E. 2008. Protein synthesis inhibition and memory: Formation vs. amnesia. Neurobiol. Learn. Mem. 89: 201-211.
29. Goshen, I., Kreisel, T., Ounallah-Saad, H., Renbaum, P., Zalzstein, Y., Ben-Hur, T., Levy-Lahad, E., and Yirmiya, R. 2007. A dual role for interleukin-1 in hippocampal-dependent memory processes. Psychoneuroendocrino. 32: 1106-1115. (Pubitemid 350086829)
30. Hein, A.M., Stutzman, D.L., Bland, S.T., Barrientos, R.M., Watkins, L.R., Rudy, J.W., and Maier, S.F. 2007. Prostaglandins are necessary and sufficient to induce contextual fear learning impairments after interleukin-1 β injections into the dorsal hippocampus. Neuroscience 150: 754-763. (Pubitemid 350235798)
31. Hernandez, P.J. and Abel, T. 2008. The role of protein synthesis in memory consolidation: Progress amid decades of debate. Neurobiol. Learn. Mem. 89: 293-311.
32. Huber, S.J., Shulman, H.G., Paulson, G.W., and Shuttleworth, E.C. 1989. Dose-dependent memory impairment in Parkinson's disease. Neurology 39: 438-440. (Pubitemid 19094747)
33. Huff, N.C., Wright-Hardesty, K.J., Higgins, E.A., Matus-Amat, P., and Rudy, J.W. 2005. Context pre-exposure obscures amygdala modulation of contextual-fear conditioning. Learn. Mem. 12: 456-460. (Pubitemid 41397205)
34. Hughes, P.E., Alexi, T., and Dragunow, M. 1997. Cycloheximide phase-shifts, but does not prevent, de novo Krox-24 protein expression. Neuroreport 8: 3263-3266. (Pubitemid 27461378)
35. Izquierdo, L.A., Barros, D.M., Vianna, M.R.M., Coitinho, A., Silva, T.D.E., Choi, H., Moletta, B., Medina, J.H., and Izquierdo, I. 2002. Molecular pharmacological dissection of short- and long-term memory. Cell. Mol. Neurobiol. 22: 269-287. (Pubitemid 35364886)
36. Kandel, E.R. 2001. The molecular biology of memory storage: A dialogue between genes and synapses. Science 294: 1030-1038. (Pubitemid 33041851)
37. Klann, E. and Sweatt, J.D. 2008. Altered protein synthesis is a trigger for long-term memory formation. Neurobiol. Learn. Mem. 89: 247-259.
38. Levenson, J.M. and Sweatt, J.D. 2005. Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 6: 108-118. (Pubitemid 40188945)
39. Liang, K.C., McGaugh, J.L., and Yao, H.Y. 1990. Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Res. 508: 225-233. (Pubitemid 20063454)
40. Martinez, J.L., Jenson, R.A., and McGaugh, J.L. 1981. Attenuation of experimentally induced amnesia. Prog. Neurobiol. 16: 155-186.
41. McHugh, T.J. and Tonegawa, S. 2007. Spatial exploration is required for the formation of contextual fear memory. Behav. Neurosci. 121: 335-339. (Pubitemid 47445084)
42. Milekic, M.H., Brown, S.D., Castellini, C., and Alberini, C.M. 2006. Persistent disruption of an established morphine conditioned place preference. J. Neurosci. 26: 3010-3020.
43. Milekic, M.H., Pollonini, G., and Alberini, C.M. 2007. Temporal requirement of C/EBPb in the amygdala following reactivation but not acquisition of inhibitory avoidance. Learn. Mem. 14: 504-511. (Pubitemid 47204849)
44. Morice, E., Billard, J.M., Denis, C., Mathieu, F., Betancur, C., Epelbaum, J., Giros, B., and Nosten-Bertrand, M. 2007. Parallel loss of hippocampal LTD and cognitive flexibility in a genetic model of hyperdopaminergia. Neuropsychopharmacol. 32: 2108-2116. (Pubitemid 47417702)
45. Morris, R.G., Inglis, J., Ainge, J.A., Olverman, H.J., Tulloch, J., Dudai, Y., and Kelly, P.A. 2006. Memory reconsolidation: Sensitivity of spatial memory to inhibition of protein synthesis in dorsal hippocampus during encoding and retrieval. Neuron 50: 479-489.
46. Nader, K. 2003. Memory traces unbound. Trends Neurosci. 26: 65-72. (Pubitemid 36110540)
47. Nader, K., Schafe, G.E., and LeDoux, J.E. 2000. The labile nature of consolidation theory. Nat. Rev. Neurosci. 1: 216-219.
48. Parsons, R.G., Gafford, G.M., Baruch, D.E., Riedner, B.A., and Helmstetter, F.J. 2006. Long-term stability of fear memory depends on the synthesis of protein but not mRNA in the amygdala. Eur. J. Neurosci. 23: 1853-1859.
49. Quartermain, D., Freedman, L.S., Botwinick, C.Y., and Gutwein, B.M. 1977. Reversal of cycloheximide-induced amnesia by adrenergic receptor stimulation. Pharmacol. Biochem. Behav. 7: 259-267. (Pubitemid 8202790)
50. Quevedo, J., Vianna, M., Daroit, D., Born, A.G., Kuyven, C.R., Roesler, R., and Quillfeldt, J.A. 1998. L-type voltage-dependent calcium channel blocker nifedipine enhances memory retention when infused into the hippocampus. Neurobiol. Learn. Mem. 69: 320-325. (Pubitemid 28374564)
51. Quevedo, J., Vianna, M.R., Roesler, R., de-Paris, F., Izquierdo, I., and Rose, S.P. 1999. Two time windows of anisomycin-induced amnesia for inhibitory avoidance training in rats: Protection from amnesia by pretraining but not pre-exposure to the task apparatus. Learn. Mem. 6:600-607.
52. Quevedo, J., Vianna, M.R., Martins, M.R., Barichello, T., Medina, J.H., Roesler, R., and Izquierdo, I. 2004. Protein synthesis, PKA, and MAP kinase are differentially involved in short- and long-term memory in rats. Behav. Brain Res. 154: 339-343. (Pubitemid 39093984)
53. Radulovic, J. and Tronson, N.C. 2008. Protein synthesis inhibitors, gene superinduction and memory: Too little or too much protein? Neurobiol. Learn. Mem. 89: 212-218.
54. Rodrigues, S.M., Schafe, G.E., and LeDoux, J.E. 2004. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44: 75-91. (Pubitemid 39348831)
55. Roozendaal, B., Nguyen, B.T., Power, A.E., and McGaugh, J.L. 1999. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc. Natl. Acad. Sci. 96: 11642-11647. (Pubitemid 29487434)
56. Rosenblum, K., Meiri, N., and Dudai, Y. 1993. Taste memory: The role of protein synthesis in gustatory cortex. Behav. Neural Biol. 59: 49-56.
57. Routtenberg, A. 2008. The substrate for long-lasting memory: If not protein synthesis, then what? Neurobiol. Learn. Mem. 89: 225-233.
58. Routtenberg, A. and Rekart, J.L. 2005. Post-translational protein modification as the substrate for long-lasting memory. Trends Neurosci. 28: 12-19. (Pubitemid 40038797)
59. Rudy, J.W. 2008. Is there a baby in the bathwater? Maybe: Some methodological issues for the de novo protein synthesis hypothesis. Neurobiol. Learn. Mem. 89: 219-224.
60. Rudy, J.W. and Matus-Amat, P. 2005. The ventral hippocampus supports a memory representation of context and contextual fear conditioning: Implications for a unitary function of the hippocampus. Behav. Neurosci. 119: 154-163. (Pubitemid 40279506)
61. Rudy, J.W., Barrientos, R.M., and O'Reilly, R.C. 2002. Hippocampal formation supports conditioning to memory of a context. Behav. Neurosci. 116: 530-538.
62. Rudy, J.W., Biedenkapp, J.C., Moineau, J., and Bolding, K. 2006. Anisomycin and the reconsolidation hypothesis. Learn. Mem. 13: 1-3. (Pubitemid 43200811)
63. Santini, E., Ge, H., Ren, K., Peña de Ortiz, S., and Quirk, G.J. 2004. Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J. Neurosci. 24: 5705-5710. (Pubitemid 38857224)
64. Schafe, G.E. and LeDoux, J.E. 2000. Memory consolidation of auditory Pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala. J. Neurosci. 20: 1-5.
65. Sharma, S.K. and Carew, T.J. 2004. The roles of MAPK cascades in synaptic plasticity and memory in Aplysia: Facilitatory effects and inhibitory constraints. Learn. Mem. 11: 373-378. (Pubitemid 39079694)
66. Siegel, S. 1956. Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York.
67. Stefani, M.R. and Gold, P.E. 1998. Intra-septal injections of glucose and glibenclamide attenuate galanin-induced spontaneous alternation performance deficits in the rat. Brain Res. 813: 50-56. (Pubitemid 29012516)
68. Taubenfeld, S.M., Milekic, M.H., Monti, B., and Alberini, C.M. 2001. The consolidation of new but not reactivated memory requires hippocampal C/EBPb. Nat. Neurosci. 4: 813-818. (Pubitemid 32702513)
69. Torocsik, B. and Szeberenyi, J. 2000a. Anisomycin affects both pro- and antiapoptotic mechanisms in PC12 cells. Biochem. Biophys. Res. Commun. 278: 550-556.
70. Torocsik, B. and Szeberenyi, J. 2000b. Anisomycin uses multiple mechanisms to stimulate mitogen-activated protein kinases and gene expression and to inhibit neuronal differentiation in PC12 phaeochromocytoma cells. Eur. J. Neurosci. 12: 527-532. (Pubitemid 30142753)
71. Touzani, K., Puthanveettil, S.V., and Kandel, E.R. 2007. Consolidation of learning strategies during spatial working memory task requires protein synthesis in the prefrontal cortex. Proc. Natl. Acad. Sci. 104: 5632-5637. (Pubitemid 47175732)
72. Wanisch, K. and Wotjak, C.T. 2008. Time course and efficiency of protein synthesis inhibition following intracerebral and systemic anisomycin treatment. Neurobiol. Learn. Mem. 90: 485-494.
73. Westerink, B.H.C. and Timmerman, W. 1999. Do neurotransmitters sampled by brain microdialysis reflect functional release? Anal. Chim. Acta 379: 263-274.
74. Xu, J., Kang, N., Jiang, L., Nedergaard, M., and Kang, J. 2005. Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J. Neurosci. 25: 1750-1760. (Pubitemid 40279280)