SSRIs and conditioned fear

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 35, Issue 8, 2011, Pages 1810-1819

  Inoue, Takeshi ^a   Kitaichi, Yuji ^a   Koyama, Tsukasa ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Amygdala; Conditioned freezing; Contextual conditioned fear; Hippocampus; Selective serotonin reuptake inhibitor; Serotonin (5 HT)

Indexed keywords

1 (2 METHOXYPHENYL) 4 (4 PHTHALIMIDOBUTYL)PIPERAZINE; 2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 5 HYDROXYTRYPTOPHAN; BENSERAZIDE; BENZODIAZEPINE; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; BUSPIRONE; CITALOPRAM; DIAZEPAM; ESCITALOPRAM; FLESINOXAN; FLUOXETINE; FLUVOXAMINE; IPSAPIRONE; KETANSERIN; MIDAZOLAM; MILNACIPRAN; MONOAMINE OXIDASE INHIBITOR; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; N [4 METHOXY 3 (4 METHYL 1 PIPERAZINYL)PHENYL] 2' METHYL 4' (5 METHYL 1,2,4 OXADIAZOL 3 YL)[1,1' BIPHENYL] 4 CARBOXAMIDE; N TERT BUTYL 3 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL] 2 PHENYLPROPIONAMIDE; NORADRENALIN UPTAKE INHIBITOR; PAROXETINE; SEROTONIN 1A AGONIST; SEROTONIN 2 ANTAGONIST; SEROTONIN NORADRENALIN REUPTAKE INHIBITOR; SEROTONIN UPTAKE INHIBITOR; TANDOSPIRONE; TRICYCLIC ANTIDEPRESSANT AGENT;

AMYGDALOID NUCLEUS; ANXIETY DISORDER; CONDITIONED FEAR; FEAR; FREEZING; HIPPOCAMPUS; HUMAN; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; LOW DRUG DOSE; NEUROCHEMISTRY; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; REVIEW; SEROTONIN METABOLISM; SEROTONINERGIC SYSTEM; STARTLE REFLEX; TRANQUILIZING ACTIVITY;

AMYGDALA; ANIMALS; CONDITIONING, CLASSICAL; FEAR; HIPPOCAMPUS; SEROTONIN UPTAKE INHIBITORS;

EID: 82455218953     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2011.09.002     Document Type: Review

References (82)

1. Avanzi V., Silva R.C., Macedo C.E., Brandao M.L. 5-HT mechanisms of median raphe nucleus in the conditioned freezing caused by light/foot-shock association. Physiol Behav 2003, 78:471-477.
2. Bandelow B., Zohar J., Hollander E., Kasper S., Moller H.J., Allgulander C., et al. World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for the pharmacological treatment of anxiety, obsessive-compulsive and post-traumatic stress disorders - first revision. World J Biol Psychiatry 2008, 9:248-312.
3. Bauer M., Döpfmer S. Lithium augmentation in treatment-resistant depression: meta-analysis of placebo-controlled studies. J Clin Psychopharmacol 1999, 19:427-434.
4. Beck C.H., Fibiger H.C. Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment. J Neurosci 1995, 15:709-720.
5. Beyer C.E., Boikess S., Luo B., Dawson L.A. Comparison of the effects of antidepressants on norepinephrine and serotonin concentrations in the rat frontal cortex: an in-vivo microdialysis study. J Psychopharmacol 2002, 16:297-304.
6. Borsini F., Podhorna J., Marazziti D. Do animal models of anxiety predict anxiolytic-like effects of antidepressants?. Psychopharmacology (Berl) 2002, 163:121-141.
7. Burghardt N.S., Sullivan G.M., McEwen B.S., Gorman J.M., LeDoux J.E. The selective serotonin reuptake inhibitor citalopram increases fear after acute treatment but reduces fear with chronic treatment: a comparison with tianeptine. Biol Psychiatry 2004, 55:1171-1178.
8. 2C receptor antagonist. Biol Psychiatry 2007, 62:1111-1118.
9. Bymaster F.P., Zhang W., Carter P.A., Shaw J., Chernet E., Phebus L., et al. Fluoxetine, but not other selective serotonin uptake inhibitors, increases norepinephrine and dopamine extracellular levels in prefrontal cortex. Psychopharmacology (Berl) 2002, 160:353-361.
10. Campeau S., Hayward M.D., Hope B.T., Rosen J.B., Nestler E.J., Davis M. Induction of the c-fos proto-oncogene in rat amygdala during unconditioned and conditioned fear. Brain Res 1991, 565:349-352.
11. Cassella J.V., Davis M. Fear-enhanced acoustic startle is not attenuated by acute or chronic imipramine treatment in rats. Psychopharmacology (Berl) 1985, 87:278-282.
12. Chaput Y., de Montigny C., Blier P. Effects of a selective 5-HT reuptake blocker, citalopram, on the sensitivity of 5-HT autoreceptors: electrophysiological studies in the rat brain. Naunyn Schmiedebergs Arch Pharmacol 1986, 333:342-348.
13. Conti L.H., MacIver C.R., Ferkany J.W., Abreu M.E. Footshock-induced freezing behavior in rats as a model for assessing anxiolytics. Psychopharmacology (Berl) 1990, 102:492-497.
14. Davis M. Neural circuitry of anxiety and stress disorders. Neuropsychopharmacology - 5th generation of progress 2002, 931-951. Lippincott Williams & Wilkins, Philadelphia. K.L. Davis, D. Charney, J.T. Coyle, C. Nemeroff (Eds.).
15. Davis M., Falls W.A., Campeau S., Kim M. Fear-potentiated startle: a neural and pharmacological analysis. Behav Brain Res 1993, 58:175-198.
16. Ehrlich I., Humeau Y., Grenier F., Ciocchi S., Herry C., Luthi A. Amygdala inhibitory circuits and the control of fear memory. Neuron 2009, 62:757-771.
17. Erikkson E., Humble M. Serotonin in psychiatric pathophysiology. A review of data from experimental and clinical research. Progress in basic clinical pharmacology 1990, 66-119. Karger, Basel. R. Pohl, S. Gershon (Eds.).
18. Fallon J.H., Ciofi P. Distribution of monoamines within the amygdala. The amygdala: a functional analysis 2000, 97-114. Oxford University Press, Oxford. 2nd ed. J. Aggleton (Ed.).
19. Fanselow M.S. Conditioned and unconditional components of post-shock freezing. Pavlov J Biol Sci 1980, 15:177-182.
20. Fanselow M.S., Helmstetter F.J. Conditional analgesia, defensive freezing, and benzodiazepines. Behav Neurosci 1988, 102:233-243.
21. 1B receptors with WAY 100,635 and GR 127,935. J Neurochem 1997, 68:1159-1163.
22. Grillon C., Levenson J., Pine D.S. A single dose of the selective serotonin reuptake inhibitor citalopram exacerbates anxiety in humans: a fear-potentiated startle study. Neuropsychopharmacology 2007, 32:225-231.
23. Grillon C., Chavis C., Covington M.F., Pine D.S. Two-week treatment with the selective serotonin reuptake inhibitor citalopram reduces contextual anxiety but not cued fear in healthy volunteers: a fear-potentiated startle study. Neuropsychopharmacology 2009, 34:964-971.
24. Handley S.L., McBlane J.W. 5HT drugs in animal models of anxiety. Psychopharmacology (Berl) 1993, 112:13-20.
25. Hashimoto S., Inoue T., Koyama T. Serotonin reuptake inhibitors reduce conditioned fear stress-induced freezing behavior in rats. Psychopharmacology (Berl) 1996, 123:182-186.
26. 1A receptor antagonists with an SSRI in conditioned fear stress-induced freezing behavior. Pharmacol Biochem Behav 1997, 58:471-475.
27. Hashimoto S., Inoue T., Koyama T. Effects of conditioned fear stress on serotonin neurotransmission and freezing behavior in rats. Eur J Pharmacol 1999, 378:23-30.
28. Hashimoto S., Inoue T., Muraki I., Koyama T. Effects of acute citalopram on the expression of conditioned freezing in naive versus chronic citalopram-treated rats. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:113-117.
29. Herman J.P., Guillonneau D., Dantzer R., Scatton B., Semerdjian-Rouquier L., Le Moal M. Differential effects of inescapable footshocks and of stimuli previously paired with inescapable footshocks on dopamine turnover in cortical and limbic areas of the rat. Life Sci 1982, 30:2207-2214.
30. Inoue T., Koyama T., Yamashita I. Effect of conditioned fear stress on serotonin metabolism in the rat brain. Pharmacol Biochem Behav 1993, 44:371-374.
31. Inoue T., Tsuchiya K., Koyama T. Regional changes in dopamine and serotonin activation with various intensity of physical and psychological stress in the rat brain. Pharmacol Biochem Behav 1994, 49:911-920.
32. Inoue T., Hashimoto S., Tsuchiya K., Izumi T., Ohmori T., Koyama T. Effect of citalopram, a selective serotonin reuptake inhibitor, on the acquisition of conditioned freezing. Eur J Pharmacol 1996, 311:1-6.
33. Inoue T., Tsuchiya K., Koyama T. Serotonergic activation reduces defensive freezing in the conditioned fear paradigm. Pharmacol Biochem Behav 1996, 53:825-831.
34. Inoue T., Tsuchiya K., Koyama T. Effects of typical and atypical antipsychotic drugs on freezing behavior induced by conditioned fear. Pharmacol Biochem Behav 1996, 55:195-201.
35. Inoue T., Hashimoto S., Izumi T., Maki Y., Muraki I., Koyama T. Effect of repeated SSRI on the acquisition of conditioned freezing. 28th annual meeting of Japanese Society of Neuropsychopharmacology (Abstract), Tokyo 1998.
36. Inoue T., Hashimoto S., Izumi T., Maki Y., Muraki I., Li X.B., et al. Serotonergic neurotransmission and defensive freezing in the conditioned fear stress paradigm. Affective minds 2000, 91-100. Elsevier Science, Amsterdam. G. Hatano, N. Okada, H. Tanabe (Eds.).
37. Inoue T., Li X.B., Abekawa T., Kitaichi Y., Izumi T., Nakagawa S., et al. Selective serotonin reuptake inhibitor reduces conditioned fear through its effect in the amygdala. Eur J Pharmacol 2004, 497:311-316.
38. Inoue T., Nakagawa S., Izumi T., Kitaichi Y., Koyama T. Effect of combined treatment with noradrenaline and serotonin reuptake inhibitors on conditioned freezing. Eur J Pharmacol 2006, 540:91-95.
39. Izumi T., Inoue T., Kitaichi Y., Nakagawa S., Koyama T. Target brain sites of the anxiolytic effect of citalopram, a selective serotonin reuptake inhibitor. Eur J Pharmacol 2006, 534:129-132.
40. Izumi T., Boku S., Shinmin W., Inoue T., Konno K., Yamaguchi T., et al. Retrieval of conditioned fear activates the basolateral and intercalated nucleus of amygdala. J Neurosci Res 2011, 89:773-790.
41. Johnson E.W., Wolfe B.B., Molinoff P.B. Regulation of subtypes of beta-adrenergic receptors in rat brain following treatment with 6-hydroxydopamine. J Neurosci Official J Soc Neurosci 1989, 9:2297-2305.
42. Joordens R.J., Hijzen T.H., Peeters B.W., Olivier B. Fear-potentiated startle response is remarkably similar in two laboratories. Psychopharmacology (Berl) 1996, 126:104-109.
43. Kakui N., Yokoyama F., Yamauchi M., Kitamura K., Imanishi T., Inoue T., et al. Anxiolytic-like profile of mirtazapine in rat conditioned fear stress model: functional significance of 5-hydroxytryptamine 1A receptor and alpha1-adrenergic receptor. Pharmacol Biochem Behav 2009, 92:393-398.
44. Kawahara H., Kawahara Y., Yoshida M., Yokoo H., Nishi M., Tanaka M. Serotonin release in the rat amygdala during exposure to emotional stress. Serotonin in the central nervous system and periphery 1995, 89-96. Elsevier Science, Amsterdam. A. Tanaka, G. Curzon (Eds.).
45. Kitaichi K., Minami Y., Amano M., Yamada K., Hasegawa T., Nabeshima T. The attenuation of suppression of motility by triazolam in the conditioned fear stress task is exacerbated by ethanol in mice. Life Sci 1995, 57:743-753.
46. Kitaichi Y., Inoue T., Nakagawa S., Izumi T., Koyama T. Effect of co-administration of subchronic lithium pretreatment and acute MAO inhibitors on extracellular monoamine levels and the expression of contextual conditioned fear in rats. Eur J Pharmacol 2006, 532:236-245.
47. LeDoux J.E. The amygdala and emotion: a view through fear. The amygdala: a functional analysis 2000, 289-310. Oxford University Press, Oxford. 2nd ed. J. Aggleton (Ed.).
48. Li X.B., Inoue T., Hashimoto S., Koyama T. Effect of chronic administration of flesinoxan and fluvoxamine on freezing behavior induced by conditioned fear. Eur J Pharmacol 2001, 425:43-50.
49. 1A receptors in the hippocampus and amygdala. Eur J Pharmacol 2006, 532:74-80.
50. Lowry C.A., Johnson P.L., Hay-Schmidt A., Mikkelsen J., Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 2005, 8:233-246.
51. Maki Y., Inoue T., Izumi T., Muraki I., Ito K., Kitaichi Y., et al. Monoamine oxidase inhibitors reduce conditioned fear stress-induced freezing behavior in rats. Eur J Pharmacol 2000, 406:411-418.
52. Miyamoto J., Tsuji M., Takeda H., Nawa H., Matsumiya T. Pretreatment with diazepam suppresses the reduction in defensive freezing behavior induced by fluvoxamine in the conditioned fear stress paradigm in mice. Eur J Pharmacol 2000, 409:81-84.
53. Montezinho L.P., Miller S., Plath N., Jensen N.H., Karlsson J.J., Witten L., et al. The effects of acute treatment with escitalopram on the different stages of contextual fear conditioning are reversed by atomoxetine. Psychopharmacology (Berl) 2010, 212:131-143.
54. Mueller D., Cahill S.P. Noradrenergic modulation of extinction learning and exposure therapy. Behav Brain Res 2010, 208:1-11.
55. Muraki I., Inoue T., Hashimoto S., Izumi T., Ito K., Ohmori T., et al. Effect of subchronic lithium carbonate treatment on anxiolytic-like effect of citalopram and MKC-242 in conditioned fear stress in the rat. Eur J Pharmacol 1999, 383:223-229.
56. Muraki I., Inoue T., Hashimoto S., Izumi T., Ito K., Koyama T. Effect of subchronic lithium treatment on citalopram-induced increases in extracellular concentrations of serotonin in the medial prefrontal cortex. J Neurochem 2001, 76:490-497.
57. 1B/1D receptor antagonist GR 127,935 on anxiolytic effect of citalopram in conditioned fear stress in the rat. Eur J Pharmacol 2008, 586:171-178.
58. Nakamura K., Kurasawa M. Anxiolytic effects of aniracetam in three different mouse models of anxiety and the underlying mechanism. Eur J Pharmacol 2001, 420:33-43.
59. Nishikawa H., Inoue T., Izumi T., Koyama T. Synergistic effects of tandospirone and selective serotonin reuptake inhibitors on the contextual conditioned fear stress response in rats. Eur Neuropsychopharmacol 2007, 17:643-650.
60. Nishikawa H., Inoue T., Masui T., Izumi T., Koyama T. Effects of cytochrome P450 (CYP) 3A4 inhibitors on the anxiolytic action of tandospirone in rat contextual conditioned fear. Prog Neuropsychopharmacol Biol Psychiatry 2007, 31:926-931.
61. Radja F., Laporte A.M., Daval G., Verge D., Gozlan H., Hamon M. Autoradiography of serotonin receptor subtypes in the central nervous system. Neurochem Int 1991, 18:1-15.
62. 1A agonist, in three stress paradigms: immobilization, forced swim and conditioned fear. Brain Res 1992, 580:205-214.
63. Sacchetti B., Lorenzini C.A., Baldi E., Tassoni G., Bucherelli C. Auditory thalamus, dorsal hippocampus, basolateral amygdala, and perirhinal cortex role in the consolidation of conditioned freezing to context and to acoustic conditioned stimulus in the rat. J Neurosci 1999, 19:9570-9578.
64. Santos J.M., Martinez R.C., Brandao M.L. Effects of acute and subchronic treatments with fluoxetine and desipramine on the memory of fear in moderate and high-intensity contextual conditioning. Eur J Pharmacol 2006, 542:121-128.
65. 1B receptor antagonists on extracellular 5-HT in rat frontal cortex in vivo. Br J Pharmacol 1997, 121:941-946.
66. Sotres-Bayon F., Cain C.K., LeDoux J.E. Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol Psychiatry 2006, 60:329-336.
67. Spennato G., Zerbib C., Mondadori C., Garcia R. Fluoxetine protects hippocampal plasticity during conditioned fear stress and prevents fear learning potentiation. Psychopharmacology (Berl) 2008, 196:583-589.
68. 3 receptor-mediated excitation in different subdivisions of the rat amygdala. Synapse 2000, 38:328-337.
69. 1A receptor-related anxiolytics. Trends Pharmacol Sci 1987, 8:432-437.
70. Unnerstall J.R., Fernandez I., Orensanz L.M. The alpha-adrenergic receptor: radiohistochemical analysis of functional characteristics and biochemical differences. Pharmacol Biochem Behav 1985, 22:859-874.
71. Van Dijken H.H., Van der Heyden J.A., Mos J., Tilders F.J. Inescapable footshocks induce progressive and long-lasting behavioural changes in male rats. Physiol Behav 1992, 51:787-794.
72. Watson J., Rayner R. Conditioned emotional reactions. J Exp Psychol 1920, 3:1-14.
73. Wilensky A.E., Schafe G.E., Kristensen M.P., LeDoux J.E. Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning. J Neurosci 2006, 26:12,387-12,396.
74. Winslow J.T., Noble P.L., Davis M. Modulation of fear-potentiated startle and vocalizations in juvenile rhesus monkeys by morphine, diazepam, and buspirone. Biol Psychiatry 2007, 61:389-395.
75. Wise R.A., Hoffman D.C. Localization of drug reward mechanisms by intracranial injections. Synapse 1992, 10:247-263.
76. Wolpe J. The practice of behavioral therapy 1969, Pergamon Press, New York.
77. 2 receptor subtype mRNAs in rat brain. J Comp Neurol 1995, 351:357-373.
78. Yokoyama M., Suzuki E., Sato T., Maruta S., Watanabe S., Miyaoka H. Amygdalic levels of dopamine and serotonin rise upon exposure to conditioned fear stress without elevation of glutamate. Neurosci Lett 2005, 379:37-41.
79. Yoshioka M., Matsumoto M., Togashi H., Saito H. Effects of conditioned fear stress on 5-HT release in the rat prefrontal cortex. Pharmacol Biochem Behav 1995, 51:515-519.
80. Yoshioka M., Matsumoto M., Togashi H., Saito H. Effect of conditioned fear stress on dopamine release in the rat prefrontal cortex. Neurosci Lett 1996, 209:201-203.
81. Zhang Y., Raap D.K., Garcia F., Serres F., Ma Q., Battaglia G., et al. Long-term fluoxetine produces behavioral anxiolytic effects without inhibiting neuroendocrine responses to conditioned stress in rats. Brain Res 2000, 855:58-66.
82. Zohar J., Westenberg H.G. Anxiety disorders: a review of tricyclic antidepressants and selective serotonin reuptake inhibitors. Acta Psychiatr Scand Suppl 2000, 403:39-49.