Previous stress Attenuates the Susceptibility to Midazolam's Disruptive Effect on Fear Memory Reconsolidation: Influence of Pre-Reactivation D-Cycloserine Administration

Neuropsychopharmacology

Volumn 35, Issue 5, 2010, Pages 1097-1108

  Bustos, Silvia Gabriela ^a   Giachero, Marcelo ^a   Maldonado, Héctor ^b   Molina, Víctor Alejandro ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b INSTITUTO DE FISIOLOGÍA   (Argentina)

Author keywords

D cyloserine; Fear memory; Midazolam; Reactivation reconsolidation; Stress

Indexed keywords

CYCLOSERINE; MIDAZOLAM; N METHYL DEXTRO ASPARTIC ACID; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL RESEARCH; CONTROLLED STUDY; DRUG EFFECT; DRUG SENSITIVITY; FEAR; INFORMATION RETRIEVAL; LEARNING; MALE; MEMORY; MEMORY DISORDER; MENTAL INSTABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS; TRAINING;

ANIMALS; CONDITIONING, CLASSICAL; CYCLOSERINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FEAR; GABA MODULATORS; MALE; MEMORY; MIDAZOLAM; NEUROTRANSMITTER AGENTS; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 77949540997     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2009.215     Document Type: Article

References (76)

1. Adamec RE, Blundell J, Burton P (2005). Neural circuit changes mediating lasting brain and behavioral response to predator stress. Neurosci Biobehav Rev 29: 1225-1241.
2. Akirav I, Maroun M (2007). The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear. Neural Plast 2007: 30873.
3. Alberini CM (2005). Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes? Trends Neurosci 28: 51-56.
4. Alberini CM, Milekic MH, Tronel S (2006). Mechanisms of memory stabilization and de-stabilization. Cell Mol Life Sci 63: 999-1008.
5. Anokhin KV, Tiunova AA, Rose SP (2002). Reminder effects: reconsolidation or retrieval deficit? Pharmacological dissection with protein synthesis inhibitors following reminder for a passive-avoidance task in young chicks. Eur J Neurosci 15: 1759-1765.
6. Baldi E, Lorenzini CA, Bucherelli C (2004). Footshock intensity and generalization in contextual and auditory-cued fear conditioning in the rat. Neurobiol Learn Mem 81: 162-166.
7. Ben Mamou C, Gamache K, Nader K (2006). NMDA receptors are critical for unleashing consolidated auditory fear memories. Nat Neurosci 9: 1237-1239.
8. Bertotto ME, Bustos SG, Molina VA, Martijena ID (2006). Influence of ethanol withdrawal on fear memory: effect of D-cycloserine. Neuroscience 142: 979-990.
9. Biedenkapp JC, Rudy JW (2007). Context preexposure prevents forgetting of a contextual fear memory: implication for regional changes in brain activation patterns associated with recent and remote memory tests. Learn Mem 14: 200-203.
10. Bignante EA, Rodriguez Manzanares PA, Mlewski EC, Bertotto ME, Bussolino DF, Paglini G. et al (2008). Involvement of septal Cdk5 in the emergence of excessive anxiety induced by stress. Eur Neuropsychopharmacol 18: 578-588.
11. Bisaz R, Conboy L, Sandi C (2008). Learning under stress: a role for the neural cell adhesion molecule NCAM. Neurobiol Learn Mem 91: 333-342.
12. Blanchard RJ, Blanchard DC (1969). Passive and active reactions to fear-eliciting stimuli. J Comp Physiol Psychol 68: 129-135.
13. Bovet D, Bovet-Nitti F, Oliverio A (1966). Short and long term memory in two inbred strains of mice. Life Sci 5: 415-420.
14. Brioni JD, McGaugh JL (1988). Post-training administration of GABAergic antagonists enhances retention of aversively motivated tasks. Psychopharmacology (Berl) 96: 505-510.
15. Brioni JD, O'Neill AB, Kim DJ, Decker MW (1993). Nicotinic receptor agonists exhibit anxiolytic-like effects on the elevated plus-maze test. Eur J Pharmacol 238: 1-8.
16. Bustos SG, Maldonado H, Molina VA (2006). Midazolam disrupts fear memory reconsolidation. Neuroscience 139: 831-842.
17. Bustos SG, Maldonado H, Molina VA (2009). Disruptive effect of midazolam on fear memory reconsolidation: decisive influence of reactivation time span and memory age. Neuropsychophar-macology 34: 446-457.
18. Cahill L, McGaugh JL (1998). Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci 21: 294-299.
19. Cancela LM, Volosin M, Molina VA (1988). Chronic stress attenuation of alpha 2-adrenoceptor reactivity is reversed by naltrexone. Pharmacol Biochem Behav 31: 33-35.
20. Castellano C, Introini-Collison IB, Pavone F, McGaugh JL (1989). Effects of naloxone and naltrexone on memory consolidation in CD1 mice: involvement of GABAergic mechanisms. Pharmacol Biochem Behav 32: 563-567.
21. Castellano C, McGaugh JL (1989). Retention enhancement with post-training picrotoxin: lack of state dependency. Behav Neural Biol 51: 165-170.
22. Chapouthier G, Venault P (2002). GABA-A receptor complex and memory processes. Curr Top Med Chem 2: 841-851.
23. Cordero MI, Venero C, Kruyt ND, Sandi C (2003). Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Evidence for a role of corticosterone. Horm Behav 44: 338-345.
24. Dudai Y (2006). Reconsolidation: the advantage of being refocused. Curr Opin Neurobiol 16: 174-178.
25. Dudai Y, Eisenberg M (2004). Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis. Neuron 44: 93-100.
26. Forcato C, Burgos VL, Argibay PF, Molina VA, Pedreira ME, Maldonado H (2007). Reconsolidation of declarative memory in humans. Learn Mem 14: 295-303.
27. Frankland PW, Ding HK, Takahashi E, Suzuki A, Kida S, Silva AJ (2006). Stability of recent and remote contextual fear memory. Learn Mem 13: 451-457.
28. Isoardi NA, Bertotto ME, Martijena ID, Molina VA, Carrer HF (2007). Lack of feedback inhibition on rat basolateral amygdala following stress or withdrawal from sedative-hypnotic drugs. Eur J Neurosci 26: 1036-1044.
29. Isoardi NA, Martijena ID, Carrer HF, Molina VA (2004). Increased fear learning coincides with neuronal dysinhibition and facilitated LTP in the basolateral amygdala following benzodia-zepine withdrawal in rats. Neuropsychopharmacol 29: 1852-1864.
30. Izquierdo I, Da Cunha C, Huang CH, Walz R, Wolfman C, Medina JH (1990). Post-training down-regulation of memory consolidation by a GABA-A mechanism in the amygdala modulated by endogenous benzodiazepines. Behav Neural Biol 54: 105-109.
31. Jasnow AM, Huhman KL (2001). Activation of GABA(A) receptors in the amygdala blocks the acquisition and expression of conditioned defeat in Syrian hamsters. Brain Res 920: 142-150.
32. Kohda K, Harada K, Kato K, Hoshino A, Motohashi J, Yamaji T. et al (2007). Glucocorticoid receptor activation is involved in producing abnormal phenotypes of single-prolonged stress rats: a putative post-traumatic stress disorder model. Neuroscience 148: 22-33.
33. Land C, Riccio DC (1999). D-Cycloserine: effects on long-term retention of a conditioned response and on memory for contextual attributes. Neurobiol Learn Mem 72: 158-168.
34. Ledgerwood L, Richardson R, Cranney J (2003). Effects of D-cycloserine on extinction of conditioned freezing. Behav Neurosci 117: 341-349.
35. Lee JL (2008). Memory reconsolidation mediates the strengthening of memories by additional learning. Nat Neurosci 11: 1264-1266.
36. Lee JL, Di Ciano P, Thomas KL, Everitt BJ (2005). Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior. Neuron 47: 795-801.
37. Lee JL, Milton AL, Everitt BJ (2006). Reconsolidation and extinction of conditioned fear: inhibition and potentiation. J Neurosci 26: 10051-10056.
38. Lee SH, Choi JH, Lee N, Lee HR, Kim JI, Yu NK (2008). Synaptic protein degradation underlies destabilization of retrieved fear memory. Science 319: 1253-1256.
39. Luft T, Pereira GS, Cammarota M, Izquierdo I (2004). Different time course for the memory facilitating effect of bicuculline in hippocampus, entorhinal cortex, and posterior parietal cortex of rats. Neurobiol Learn Mem 82: 52-56.
40. Mao SC, Lin HC, Gean PW (2008). Augmentation of fear extinction by D-cycloserine is blocked by proteasome inhibitors. Neurop-sychopharmacology 33: 3085-3095.
41. Martijena ID, Calvo N, Volosin M, Molina VA (1997). Prior exposure to a brief restraint session facilitates the occurrence of fear in response to a conflict situation: behavioral and neurochemical correlates. Brain Res 752: 136-142.
42. Martijena ID, Rodŕiguez Manzanares PA, Lacerra C, Molina VA (2002). Gabaergic modulation of the stress response in frontal cortex and amygdala. Synapse 45: 86-94.
43. Matsuoka N, Aigner TG (1996). D-cycloserine, a partial agonist at the glycine site coupled to N-methyl-D-aspartate receptors, improves visual recognition memory in rhesus monkeys. J Pharmacol Exp Ther 278: 891-897.
44. McGaugh JL (2002). Memory consolidation and the amygdala: a systems perspective. Trends Neurosci 25: 456.
45. McGaugh JL (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27: 1-28.
46. Milekic MH, Alberini CM (2002). Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36: 521-525.
47. Monahan JB, Handelmann GE, Hood WF, Cordi AA (1989). D-cycloserine, a positive modulator of the N-methyl-D-aspartate receptor, enhances performance of learning tasks in rats. Pharmacol Biochem Behav 34: 649-653.
48. Myers KM, Davis M (2002). Behavioral and neural analysis of extinction. Neuron 36: 567-584.
49. Nader K, Schafe GE, Le Doux JE (2000). Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406: 722-726.
50. Payne JD, Jackson ED, Hoscheidt S, Ryan L, Jacobs WJ, Nadel L (2007). Stress administered prior to encoding impairs neutral but enhances emotional long-term episodic memories. Learn Mem 14: 861-868.
51. Pedreira ME, Maldonado H (2003). Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38: 863-869.
52. Pitkänen M, Sirviö J, MacDonald E, Niemi S, Ekonsalo T, Riekkinen P (1995). The effects of D-cycloserine and MK-801 on the performance of rats in two spatial learning and memory tasks. Eur Neuropsychopharmacol 5: 457-463.
53. Pussinen R, Nieminen S, Koivisto E, Haapalinna A, Riekkinen Sr P, Sirvio J (1997). Enhancement of intermediate-term memory by an alpha-1 agonist or a partial agonist at the glycine site of the NMDA receptor. Neurobiol Learn Mem 67: 69-74.
54. Quartermain D, Mower J, Rafferty MF, Herting RL, Lanthorn TH (1994). Acute but not chronic activation of the NMDA-coupled glycine receptor with D-cycloserine facilitates learning and retention. Eur J Pharmacol 257: 7-12.
55. Riccio CA, Garland BH, Cohen MJ (2007). Relations between the Test of Variables of Attention (TOVA) and the Children's Memory Scale (CMS). J Atten Disord 11: 167-171.
56. Rodŕiguez Manzanares PA, Isoardi NA, Carrer HF, Molina VA (2005). Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J Neurosci 25: 8725-8734.
57. Roozendaal B (2002). Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol Learn Mem 78: 578-595.
58. Roozendaal B, McEwen BS, Chattarji S (2009). Stress, memory and the amygdala. Nat Rev Neurosci 10: 423-433.
59. Roozendaal B, Schelling G, McGaugh JL (2008). Corticotropin-releasing factor in the basolateral amygdala enhances memory consolidation via an interaction with the beta-adrenoceptor-cAMP pathway: dependence on glucocorticoid receptor activation. J Neurosci 28: 6642-6651.
60. Rouaud E, Billard JM (2003). D-cycloserine facilitates synaptic plasticity but impairs glutamatergic neurotransmission in rat hippocampal slices. Br J Pharmacol 140: 1051-1056.
61. Sandi C (1998). The role and mechanisms of action of glucocorticoid involvement in memory storage. Neural Plast 6: 41-52.
62. Sangha S, Scheibenstock A, Lukowiak K (2003). Reconsolidation of a long-term memory in lymnaea requires new protein and RNA synthesis and the soma of right pedal dorsal 1. J Neurosci 23: 8034-8040.
63. Sara SJ (2000). Retrieval and reconsolidation: toward a neurobiol-ogy of remembering. Learn Mem 7: 73-84.
64. Shors TJ (2001). Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiol Learn Mem 75: 10-29.
65. Shors TJ, Mathew PR (1998). NMDA receptor antagonism in the lateral/basolateral but not central nucleus of the amygdala prevents the induction of facilitated learning in response to stress. Learn Mem 5: 220-230.
66. Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S (2004). Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24: 4787-4795.
67. Takahashi T, Morinobu S, Iwamoto Y, Yamawaki S (2007). Effect of paroxetine on enhanced contextual fear induced by single prolonged stress in rats. Psychopharmacology (Berl) 189: 165-173.
68. Taubenfeld SM, Riceberg JS, New AS, Alberini CM (2009). Preclinical assessment for selectively disrupting a traumatic memory via postretrieval inhibition of glucocorticoid receptors. Biol Psychiatry 65: 249-257.
69. Thompson LT, Moskal JR, Disterhoft JF (1992). Hippocampus-dependent learning facilitated by a monoclonal antibody or D-cycloserine. Nature 359: 638-641.
70. Tronson NC, Taylor JR (2007). Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci 8: 262-275.
71. Walker DL, Ressler KJ, Lu KT, Davis M (2002). Facilitation of conditioned fear extinction by systemic administration or intra-amygdala infusions of D-cycloserine as assessed with fear-potentiated startle in rats. J Neurosci 22: 2343-2351.
72. Walker MP, Brakefield T, Hobson JA, Stickgold R (2003). Dissociable stages of human memory consolidation and reconsolidation. Nature 425: 616-620.
73. Wang SH, de Oliveira Alvares L, Nader K (2009). Cellular and systems mechanisms of memory strength as a constraint on auditory fear reconsolidation. Nat Neurosci 12: 905-912.
74. Wiltgen BJ, Silva AJ (2007). Memory for context becomes less specific with time. Learn Mem 14: 313-317.
75. Yamamoto S, Morinobu S, Fuchikami M, Kurata A, Kozuru T, Yamawaki S (2008). Effects of single prolonged stress and D-cycloserine on contextual fear extinction and hippocampal NMDA receptor expression in a rat model of PTSD. Neuropsy-chopharmacology 33: 2108-2116.
76. Zhang S, Cranney J (2008). The role of GABA and anxiety in the reconsolidation of conditioned fear. Behav Neurosci 122: 1295-1305.