5-Hydroxytryptamine 2C Receptors in the Basolateral Amygdala Are Involved in the Expression of Anxiety After Uncontrollable Traumatic Stress

Biological Psychiatry

Volumn 67, Issue 4, 2010, Pages 339-345

  Christianson, John P ^a   Ragole, Thomas ^a   Amat, Jose ^a   Greenwood, Benjamin N ^a   Strong, Paul V ^a   Paul, Evan D ^a   Fleshner, Monika ^a   Watkins, Linda R ^a   Maier, Steven F ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

5 HT2c; learned helplessness; PTSD; rat; serotonin; social exploration

Indexed keywords

SEROTONIN; SEROTONIN 2C RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; CELL ACTIVITY; CELL LEVEL; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; IN VIVO STUDY; MALE; MICRODIALYSIS; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; RAT; SEROTONIN UPTAKE; SIGNAL TRANSDUCTION; TAIL FLICK TEST;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; AMINOPYRIDINES; AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANXIETY; DISEASE MODELS, ANIMAL; ELECTROSHOCK; INDOLES; MICRODIALYSIS; RATS; RECEPTOR, SEROTONIN, 5-HT2C; SEROTONIN; SEROTONIN AGONISTS; SEROTONIN ANTAGONISTS; SOCIAL BEHAVIOR; STRESS DISORDERS, TRAUMATIC;

EID: 74749086513     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2009.09.011     Document Type: Article

References (51)

1. Kessler R.C., Sonnega A., Bromet E., Hughes M., and Nelson C.B. Posttraumatic stress disorder in the National Comorbidity Survey. Arch Gen Psychiatry 52 (1995) 1048-1060
2. Davis L.L., English B.A., Ambrose S.M., and Petty F. Pharmacotherapy for post-traumatic stress disorder: A comprehensive review. Expert Opin Pharmacother 2 (2001) 1583-1595
3. Association A.P. Diagnostic and Statistical Manual of Mental Disorders. 4th ed. (2000), American Psychiatric Association, Washington, DC Text Revision.
4. Bryant R.A. Early predictors of posttraumatic stress disorder. Biol Psychiatry 53 (2003) 789-795
5. Bryant R.A., Mastrodomenico J., Felmingham K.L., Hopwood S., Kenny L., Kandris E., et al. Treatment of acute stress disorder: A randomized controlled trial. Arch Gen Psychiatry 65 (2008) 659-667
6. Maier S.F., and Watkins L.R. Stressor controllability and learned helplessness: The roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci Biobehav Rev 29 (2005) 829-841
7. Southwick S.M., Vythilingam M., and Charney D.S. The psychobiology of depression and resilience to stress: Implications for prevention and treatment. Annu Rev Clin Psychol 1 (2005) 255-291
8. Foa E.B., Zinbarg R., and Rothbaum B.O. Uncontrollability and unpredictability in post-traumatic stress disorder: An animal model. Psychol Bull 112 (1992) 218-238
9. Baratta M.V., Christianson J.P., Gomez D.M., Zarza C.M., Amat J., Masini C.V., et al. Controllable versus uncontrollable stressors bi-directionally modulate conditioned but not innate fear. Neuroscience 146 (2007) 1495-1503
10. Maier S.F. Role of fear in mediating shuttle escape learning deficit produced by inescapable shock. J Expert Psychol Anim Behav Process 16 (1990) 137-149
11. Minor T.R., Dess N.K., Ben-David E., and Chang W.C. Individual differences in vulnerability to inescapable shock in rats. J Expert Psychol Anim Behav Process 20 (1994) 402-412
12. Christianson J.P., Paul E.D., Irani M., Thompson B.M., Kubala K.H., Yirmiya R., et al. The role of prior stressor controllability and the dorsal raphe nucleus in sucrose preference and social exploration. Behav Brain Res 193 (2008) 87-93
13. Short K.R., and Maier S.F. Stressor controllability, social interaction, and benzodiazepine systems. Pharmacol Biochem Behav 45 (1993) 827-835
14. Amat J., Baratta M.V., Paul E., Bland S.T., Watkins L.R., and Maier S.F. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8 (2005) 365-371
15. Greenwood B.N., Foley T.E., Day H.E., Campisi J., Hammack S.H., Campeau S., et al. Freewheel running prevents learned helplessness/behavioral depression: Role of dorsal raphe serotonergic neurons. J Neurosci 23 (2003) 2889-2898
16. Maier S.F., Grahn R.E., and Watkins L.R. 8-OH-DPAT microinjected in the region of the dorsal raphe nucleus blocks and reverses the enhancement of fear conditioning and interference with escape produced by exposure to inescapable shock. Behav Neurosci 109 (1995) 404-412
17. Lipinski Jr. J.F., Mallya G., Zimmerman P., and Pope Jr. H.G. Fluoxetine-induced akathisia: Clinical and theoretical implications. J Clin Psychiatry 50 (1989) 339-342
18. Bagdy G., Graf M., Anheuer Z.E., Modos E.A., and Kantor S. Anxiety-like effects induced by acute fluoxetine, sertraline or m-CPP treatment are reversed by pretreatment with the 5-HT2C receptor antagonist SB-242084 but not the 5-HT1A receptor antagonist WAY-100635. Int J Neuropsychopharmacol 4 (2001) 399-408
19. Handley S.L., and McBlane J.W. 5HT drugs in animal models of anxiety. Psychopharmacology 112 (1993) 13-20
20. Burghardt N.S., Bush D.E., McEwen B.S., and LeDoux J.E. Acute selective serotonin reuptake inhibitors increase conditioned fear expression: Blockade with a 5-HT(2C) receptor antagonist. Biol Psychiatry 62 (2007) 1111-1118
21. Greenwood B.N., Strong P.V., Brooks L., and Fleshner M. Anxiety-like behaviors produced by acute fluoxetine administration in male Fischer 344 rats are prevented by prior exercise. Psychopharmacology 199 (2008) 209-222
22. File S.E., and Seth P. A review of 25 years of the Social Interaction Test. Eur J Pharmacol 463 (2003) 35-53
23. Grahn R.E., Will M.J., Hammack S.E., Maswood S., McQueen M.B., Watkins L.R., et al. Activation of serotonin-immunoreactive cells in the dorsal raphe nucleus in rats exposed to an uncontrollable stressor. Brain Res 826 (1999) 35-43
24. Lowry C.A. Functional subsets of serotonergic neurones: Implications for control of the hypothalamic-pituitary-adrenal axis. J Neuroendocrinol 14 (2002) 911-923
25. Shekhar A., Truitt W., Rainnie D., and Sajdyk T. Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety. Stress 8 (2005) 209-219
26. Walker D.L., Toufexis D.J., and Davis M. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol 463 (2003) 199-216
27. Campbell B.M., and Merchant K.M. Serotonin 2C receptors within the basolateral amygdala induce acute fear-like responses in an open-field environment. Brain Res 993 (2003) 1-9
28. Overstreet D.H., Knapp D.J., Angel R.A., Navarro M., and Breese G.R. Reduction in repeated ethanol-withdrawal-induced anxiety-like behavior by site-selective injections of 5-HT1A and 5-HT2C ligands. Psychopharmacology 187 (2006) 1-12
29. Strong P.V., Greenwood B.N., and Fleshner M. The effects of the selective 5-HT(2C) receptor antagonist SB 242084 on learned helplessness in male Fischer 344 rats. Psychopharmacology 203 (2008) 665-675
30. Amat J., Matus-Amat P., Watkins L.R., and Maier S.F. Escapable and inescapable stress differentially alter extracellular levels of 5-HT in the basolateral amygdala of the rat. Brain Res 812 (1998) 113-120
31. Christianson J.P., Benison A.M., Jennings J., Sandsmark E.K., Amat J., Kaufman R.D., et al. The sensory insular cortex mediates the stress-buffering effects of safety signals but not behavioral control. J Neurosci 28 (2008) 13703-13711
32. Matos F.F., Urban C., and Yocca F.D. Serotonin (5-HT) release in the dorsal raphe and ventral hippocampus: Raphe control of somatodendritic and terminal 5-HT release. J Neural Transm 103 (1996) 173-190
33. Kirby L.G., Rice K.C., and Valentino R.J. Effects of corticotropin-releasing factor on neuronal activity in the serotonergic dorsal raphe nucleus. Neuropsychopharmacology 22 (2000) 148-162
34. Strong P.V., Greenwood B.N., and Fleshner M. The effects of the selective 5-HT(2C) receptor antagonist SB 242084 on learned helplessness in male Fischer 344 rats. Psychopharmacology 203 (2009) 665-675
35. Navailles S., Moison D., Ryczko D., and Spampinato U. Region-dependent regulation of mesoaccumbens dopamine neurons in vivo by the constitutive activity of central serotonin2C receptors. J Neurochem 99 (2006) 1311-1319
36. Christianson J.P., Thompson B.M., Watkins L.R., and Maier S.F. Medial prefrontal cortical activation modulates the impact of controllable and uncontrollable stressor exposure on a social exploration test of anxiety. [published online ahead of print December 2]. Stress (2008)
37. Haller J., and Bakos N. Stress-induced social avoidance: A new model of stress-induced anxiety?. Physiol Behav 77 (2002) 327-332
38. Rueter L.E., Fornal C.A., and Jacobs B.L. A critical review of 5-HT brain microdialysis and behavior. Rev Neurosci 8 (1997) 117-137
39. Overstreet D.H., Knapp D.J., and Breese G.R. Accentuated decrease in social interaction in rats subjected to repeated ethanol withdrawals. Alcohol Clin Exp Res 26 (2002) 1259-1268
40. Cooper M.A., Grober M.S., Nicholas C.R., and Huhman K.L. Aggressive encounters alter the activation of serotonergic neurons and the expression of 5-HT1A mRNA in the hamster dorsal raphe nucleus. Neuroscience 161 (2009) 680-690
41. Cooper M.A., McIntyre K.E., and Huhman K.L. Activation of 5-HT1A autoreceptors in the dorsal raphe nucleus reduces the behavioral consequences of social defeat. Psychoneuroendocrinology 33 (2008) 1236-1247
42. Lanzenberger R.R., Mitterhauser M., Spindelegger C., Wadsak W., Klein N., Mien L.K., et al. Reduced serotonin-1A receptor binding in social anxiety disorder. Biol Psychiatry 61 (2007) 1081-1089
43. Lowry C.A., Johnson P.L., Hay-Schmidt A., Mikkelsen J., and Shekhar A. Modulation of anxiety circuits by serotonergic systems. Stress 8 (2005) 233-246
44. Heisler L.K., Zhou L., Bajwa P., Hsu J., and Tecott L.H. Serotonin 5-HT(2C) receptors regulate anxiety-like behavior. Genes Brain Behav 6 (2007) 491-496
45. Hackler E.A., Turner G.H., Gresch P.J., Sengupta S., Deutch A.Y., Avison M.J., et al. 5-Hydroxytryptamine 2C receptor contribution to m-chlorophenylpiperazine and N-methyl-beta-carboline-3-carboxamide-induced anxiety-like behavior and limbic brain activation. J Pharmacol Exp Ther 320 (2007) 1023-1029
46. Millan M.J. The neurobiology and control of anxious states. Prog Neurobiol 70 (2003) 83-244
47. Stutzmann G.E., and LeDoux J.E. GABAergic antagonists block the inhibitory effects of serotonin in the lateral amygdala: A mechanism for modulation of sensory inputs related to fear conditioning. J Neurosci 19 (1999) RC8
48. Rainnie D.G. Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82 (1999) 69-85
49. Huidobro-Toro J.P., Valenzuela C.F., and Harris R.A. Modulation of GABAA receptor function by G protein-coupled 5-HT2C receptors. Neuropharmacology 35 (1996) 1355-1363
50. Stein C., Davidowa H., and Albrecht D. 5-HT(1A) receptor-mediated inhibition and 5-HT(2) as well as 5-HT(3) receptor-mediated excitation in different subdivisions of the rat amygdala. Synapse 38 (2000) 328-337
51. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. 4th ed. (1998), Academic Press, New York