PTSD-like memory generated through enhanced noradrenergic activity is mitigated by a dual step pharmacological intervention targeting its reconsolidation

International Journal of Neuropsychopharmacology

Volumn 18, Issue 1, 2015, Pages

  Gazarini, Lucas ^a   Stern, Cristina A J ^a   Piornedo, Rene R ^a   Takahashi, Reinaldo N ^a   Bertoglio, Leandro J ^a  

^a FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

Author keywords

Fear generalization; Memory overconsolidation; Norepinephrine; PTSD

Indexed keywords

BETA ADRENERGIC RECEPTOR; CANNABIDIOL; CLONIDINE; CYCLOSERINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROPRANOLOL; YOHIMBINE; ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; ALPHA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; AMINO ACID RECEPTOR AFFECTING AGENT; PSYCHOTROPIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD PRESSURE MEASUREMENT; CONDITIONING; CONTROLLED STUDY; FEAR; IMAGE RETRIEVAL; INFORMATION RETRIEVAL; MALE; MEMORY CONSOLIDATION; NERVOUS SYSTEM FUNCTION; NONHUMAN; NORADRENERGIC ACTIVITY; NORADRENERGIC SYSTEM; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RAT; SYSTOLIC BLOOD PRESSURE; ANIMAL; BLOOD PRESSURE; DRUG EFFECTS; MEMORY; PHYSIOLOGY; RANDOMIZATION; REINFORCEMENT; STRESS DISORDERS, POST-TRAUMATIC; WISTAR RAT;

ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; ANIMALS; BLOOD PRESSURE; CANNABIDIOL; CLONIDINE; CYCLOSERINE; EXCITATORY AMINO ACID AGENTS; EXTINCTION, PSYCHOLOGICAL; FEAR; MALE; MEMORY; PSYCHOTROPIC DRUGS; RANDOM ALLOCATION; RATS, WISTAR; STRESS DISORDERS, POST-TRAUMATIC; YOHIMBINE;

EID: 84930276850     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyu026     Document Type: Article

References (51)

1. Adamec R, Muir C, Grimes M, Pearcey K (2007) Involvement of noradrenergic and corticoid receptors in the consolidation of the lasting anxiogenic effects of predator stress. Behav Brain Res 179:192-207.
2. Alberini CM (2011) The role of reconsolidation and the dynamic process of long-term memory formation and storage. Front Behav Neurosci 5:12.
3. Anisman H (2011) Sensitization in relation to posttraumatic stress disorder. Biol Psychiatry 70:404-405.
4. Bhuvaneswar CG, Ruskin JN, Katzman AR, Wood N, Pitman RK (2014) Pilot study of the effect of lipophilic vs. hydrophilic beta-adrenergic blockers being taken at time of intracardiac defibrillator discharge on subsequent PTSD symptoms. Neurobiol Learn Mem. 112:248-252.
5. Bustos SG, Giachero M, Maldonado H, Molina VA (2010) Previous stress attenuates the susceptibility to Midazolam's disruptive effect on fear memory reconsolidation: influence of pre-reactivation D-cycloserine administration. Neuropsychopharmacology 35:1097-1108.
6. Cain CK, Maynard GD, Kehne JH (2012) Targeting memory processes with drugs to prevent or cure PTSD. Expert Opin Investig Drugs 21:1323-1350.
7. Campos AC, Moreira FA, Gomes FV, Del Bel EA, Guimaraes FS (2012) Multiple mechanisms involved in the large-spectrum therapeutic potential of cannabidiol in psychiatric disorders. Phil Trans R Soc B 367:3364-3378.
8. Daskalakis NP, Yehuda R, Diamond DM (2013) Animal models in translational studies of PTSD. Psychoneuroendocrinology 38:1895-1911.
9. Debiec J (2012) Memory reconsolidation processes and posttraumatic stress disorder: promises and challenges of translational research. Biol Psychiatry 71:284-285.
10. Debiec J, Bush DE, LeDoux JE (2011) Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats-a possible mechanism for the persistence of traumatic memories in PTSD. Depress Anxiety 28:186-193.
11. Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55:51-86.
12. Dudai Y (2012) The restless engram: consolidations never end. Annu Rev Neurosci 35:227-247.
13. Ehlers A, Hackmann A, Michael T (2004) Intrusive re-experiencing in post-traumatic stress disorder: phenomenology, theory, and therapy. Memory 12:403-415.
14. Elzinga BM, Bremner JD (2002) Are the neural substrates of memory the final common pathway in posttraumatic stress disorder (PTSD)? J Affect Disord 70:1-17.
15. Gamache K, Pitman RK, Nader K (2012) Preclinical evaluation of reconsolidation blockade by clonidine as a potential novel treatment for posttraumatic stress disorder. Neuropsychopharmacology 37:2789-2796.
16. Gazarini L, Stern CA, Carobrez AP, Bertoglio LJ (2013) Enhanced noradrenergic activity potentiates fear memory consolidation and reconsolidation by differentially recruiting α1- and β-adrenergic receptors. Learn Mem 20:210-219.
17. Hoge EA, Worthington JJ, Nagurney JT, Chang Y, Kay EB, Feterowski CM, Katzman AR, Goetz JM, Rosasco ML, Lasko NB, Zusman RM, Pollack MH, Orr SP, Pitman RK (2012) Effect of acute posttrauma propranolol on PTSD outcome and physiological responses during script-driven imagery. CNS Neurosci Ther 18:21-27.
18. Hubbard JW, Pfister SL, Biediger AM, Herzig TC, Keeton TK (1988) The pharmacokinetic properties of yohimbine in the conscious rat. Naunyn Schmiedebergs Arch Pharmacol 337:583-587.
19. Ivanov A, Aston-Jones G (1995) Extranuclear dendrites of locus coeruleus neurons: activation by glutamate and modulation of activity by alpha adrenoceptors. J Neurophysiol 74:2427-2436.
20. Ji JZ, Wang XM, Li BM (2003) Deficit in long-term contextual fear memory induced by blockade of beta-adrenoceptors in hippocampal CA1 region. Eur J Neurosci 17:1947-1952.
21. Jovanovic T, Norrholm SD, Fennell JE, Keyes M, Fiallos AM, Myers KM, Davis M, Duncan EJ (2009) Posttraumatic stress disorder may be associated with impaired fear inhibition: relation to symptom severity. Psychiatry Res 167:151-160.
22. Kheirbek MA, Klemenhagen KC, Sahay A, Hen R (2012) Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci 15:1613-1620.
23. Kroon JA, Carobrez AP (2009). Olfactory fear conditioning paradigm in rats: effects of midazolam, propranolol or scopolamine. Neurobiol Learn Mem 91:32-40.
24. LaLumiere RT, Buen TV, McGaugh JL (2003) Post-training intrabasolateral amygdala infusions of norepinephrine enhance consolidation of memory for contextual fear conditioning. J Neurosci 23:6754-6758.
25. Lee JL, Milton AL, Everitt BJ (2006) Reconsolidation and extinction of conditioned fear: inhibition and potentiation. J Neurosci 26:10051-10056.
26. Liberzon I, Abelson JL, Flagel SB, Raz J, Young EA (1999) Neuroendocrine and psychophysiologic responses in PTSD: a symptom provocation study. Neuropsychopharmacology 21:40-50.
27. Maren S, Phan KL, Liberzon I (2013) The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14:417-428.
28. Milad MR, Pitman RK, Ellis CB, Gold AL, Shin LM, Lasko NB, Zeidan MA, Handwerger K, Orr SP, Rauch SL (2009) Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 66:1075-1082.
29. Muravieva EV, Alberini CM (2010) Limited efficacy of propranolol on the reconsolidation of fear memories. Learn Mem 17:306-313.
30. Nader K, Schafe GE, Le Doux JE (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722-726.
31. Olson VG, Rockett HR, Reh RK, Redila VA, Tran PM, Venkov HA, Defino MC, Hague C, Peskind ER, Szot P, Raskind MA (2011) The role of norepinephrine in differential response to stress in an animal model of posttraumatic stress disorder. Biol Psychiatry 70:441-448.
32. Parsons RG, Ressler KJ (2013) Implications of memory modulation for post-traumatic stress and fear disorders. Nat Neurosci 16:146-153.
33. Perry BD, Giller EL Jr, Southwick SM (1987) Altered platelet alpha 2-adrenergic binding sites in posttraumatic stress disorder. Am J Psych 144:1511-1512.
34. Pitman R, Sanders K, Zusman R, Healy A, Cheema F, Lasko N (2002) Pilot study of secondary prevention of posttraumatic stress disorder with propranolol. Biol Psychiatry 51:189-192.
35. Pitman RK (1989) Post-traumatic stress disorder, hormones, and memory. Biol Psychiatry 26:221-223.
36. Pitman RK, Rasmusson AM, Koenen KC, Shin LM, Orr SP, Gilbertson MW, Milad MR, Liberzon I (2012) Biological studies of post-traumatic stress disorder. Nat Rev Neurosci 13:769-787.
37. Przybyslawski J, Roullet P, Sara SJ (1999) Attenuation of emotional and nonemotional memories after their reactivation: role of beta adrenergic receptors. J Neurosci 19:6623-6628.
38. Quirk GJ, Mueller D (2008) Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33:56-72.
39. Sara SJ (2000) Retrieval and reconsolidation: toward a neurobiology of remembering. Learn Mem 7:73-84.
40. Sara SJ (2009) The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 10:211-223.
41. Schwabe L, Nader K, Wolf OT, Beaudry T, Pruessner JC (2012) Neural signature of reconsolidation impairments by propranolol in humans. Biol Psychiatry 71:380-386.
42. Soeter M, Kindt M (2012) Stimulation of the noradrenergic system during memory formation impairs extinction learning but not the disruption of reconsolidation. Neuropsychopharmacology 37:1204-1215.
43. Soeter M, Kindt M (2013) High trait anxiety: a challenge for disrupting fear memory reconsolidation. PLOS ONE 8:e75239.
44. Stein MB, Kerridge C, Dimsdale JE, Hoyt DB (2007) Pharmacotherapy to prevent PTSD: Results from a randomized controlled proof-of-concept trial in physically injured patients. J Trauma Stress 20:923-932.
45. Stern CA, Gazarini L, Takahashi RN, Guimaraes FS, Bertoglio LJ (2012) On disruption of fear memory by reconsolidation blockade: evidence from cannabidiol treatment. Neuropsychopharmacology 37:2132-2142.
46. Stern CA, Gazarini L, Vanvossen AC, Hames MS, Bertoglio LJ (2013) Activity in prelimbic cortex subserves fear memory reconsolidation over time. Learn Mem 21:14-20.
47. Tronel S, Feenstra MG, Sara SJ (2004) Noradrenergic action in prefrontal cortex in the late stage of memory consolidation. Learn Mem 11:453-458.
48. Vaiva G, Ducrocq F, Jezequel K, Averland B, Lestavel P, Brunet A, Marmar CR (2003) Immediate treatment with propranolol decreases posttraumatic stress disorder two months after trauma. Biol Psychiatry 54:947-949.
49. Xu W, Sudhof TC (2013) A neural circuit for memory specificity and generalization. Science 339:1290-1295.
50. Yehuda R, McFarlane AC, Shalev AY (1998) Predicting the development of posttraumatic stress disorder from the acute response to a traumatic event. Biol Psychiatry 44:1305-1313.
51. Zoladz PR, Diamond DM (2013) Current status on behavioral and biological markers of PTSD: a search for clarity in a conflicting literature. Neurosci Biobehav Rev 37:860-895.