A role for 5-HT1A receptors in the basolateral amygdala in the development of conditioned defeat in Syrian hamsters

Pharmacology Biochemistry and Behavior

Volumn 100, Issue 3, 2012, Pages 592-600

  Morrison, Kathleen E ^a   Cooper, Matthew A ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Anxiety; Defensive behavior; Fear; Serotonin; Social defeat; Stress

Indexed keywords

FLESINOXAN; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; SEROTONIN 1A RECEPTOR;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL AMYGDALA; CONDITIONED DEFEAT; CONTROLLED STUDY; DRUG EFFECT; MALE; NONHUMAN; PRIORITY JOURNAL; SOCIAL ASPECT; SYRIAN HAMSTER;

AMYGDALA; ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); CRICETINAE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MESOCRICETUS; MOLECULAR TARGETED THERAPY; NERVE TISSUE PROTEINS; NEURONS; PIPERAZINES; PYRIDINES; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN 5-HT1 RECEPTOR AGONISTS; SEROTONIN 5-HT1 RECEPTOR ANTAGONISTS; STRESS, PSYCHOLOGICAL;

MESOCRICETUS AURATUS;

EID: 83555179177     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2011.09.005     Document Type: Article

References (76)

1. E. Akimova, R. Lanzenberger, and S. Kasper The serotonin-1A receptor in anxiety disorders Biol Psychiatry 66 2009 627 635
2. H.E. Albers, K.L. Huhman, and R.L. Meisel Hormonal basis of social conflict and communication D.W. Pfaff, Hormones, Brain and Behavior 2002 Academic Press San Diego 393 433
3. R.C. Almada, K.G. Borelli, L. Albrechet-Souza, and M.L. Brandao Serotonergic mechanisms of the median raphe nucleus-dorsal hippocampus in conditioned fear: output circuit involves the prefrontal cortex and amygdala Behav Brain Res 203 2009 279 287
4. N.M. Barnes, and T. Sharp A review of central 5-HT receptors and their function Neuropharmacology 38 1999 1083 1152 (Pubitemid 29292403)
5. O. Berton, S. Aguerre, A. Sarrieau, P. Mormede, and F. Chaouloff Differential effects of social stress on central serotonergic activity and emotional reactivity in Lewis and spontaneously hypertensive rats Neuroscience 82 1998 147 159 (Pubitemid 27441535)
6. D.C. Blanchard, R.L. Spencer, S.M. Weiss, R.J. Blanchard, B.S. McEwen, and R.R. Sakai Visible burrow system as a model of chronic social stress: behavioral and neuroendocrine correlates Psychoneuroendocrinology 20 1995 117 134
7. A.C. Broiz, L.C. Oliveira, and M.L. Brandao Regulation of conditioned and unconditioned fear in rats by 5-HT1A receptors in the dorsal periacqueductal gray Pharmacol Biochem Behav 89 2008 76 84
8. B.M. Campbell, and K.M. Merchant Serotonin 2C receptors within the basolateral amygdala induce actue fear-like responses in an open-field environment Brain Res 993 2003 1 9 (Pubitemid 37464577)
9. S. Campeau, M.J. Miserendino, and M. Davis Intra-amygdala infustion of the N-methyl-D-aspartate receptor antagonist AP5 blocks acquisition but not expression of fear-potentiated startle to an auditory conditioned stimulus Behav Neurosci 106 1992 569 574
10. J.C. Compaan, L. Groenink, J. Van der Gugten, R.A.A. Maes, and B. Olivier Pretreatment with 5-HT1A receptor agonist flesinoxan attenuates Fos protein in rat hypothalamus Eur J Pharmacol 324 1997 161 168 (Pubitemid 27174601)
11. M.A. Cooper, K.E. McIntyre, and K.L. Huhman Activation of 5-HT1A autoreceptors in the dorsal raphe nucleus reduces the behavioral consequences of social defeat Psychoneuroendocrinology 33 2008 1236 1247
12. M. Davis, J.V. Cassella, and J.H. Kehne Serotonin does not mediate anxiolytic effects of buspirone in the fear-potentiated startle paradigm: comparison with 8-OH-DPAT and isapirone Psychopharmacology (Berl) 94 1988 14 20 (Pubitemid 18009057)
13. L. Dawson, and J. Watson Vilazodone: a 5-HT1A receptor agonist/serotonin transporter inhibitor for the treatment of affective disorders CNS Neurosci Ther 15 2009 107 117
14. D.E. Day, M.A. Cooper, C.M. Markham, and K.L. Huhman NR2B subunit of the NMDA receptor in the basolateral amygdala is necessary for the acquisition of conditioned defeat in Syrian hamsters Behav Brain Res 217 2011 55 59
15. M.S. Fanselow, and J. Kim Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist D, L-2-amino-5-phosphonovaleric acid to the basolateral amygdala Behav Neurosci 108 1994 210 212 (Pubitemid 24097761)
16. S.E. File, L.E. Gonzalez, and N. Andrews Comparative study of pre- and postsynaptic 5-HT1A receptor modulation of anxiety in two ethological animal tests J Neurosci 16 1996 4810 4815 (Pubitemid 26251075)
17. H.-R. Frischknecht, B. Siegfried, and P.G. Waser Learning of submissive behavior in mice: a new model Behav Processes 7 1982 235 245 (Pubitemid 13245334)
18. J. Gerwitz, and M. Davis Second-order fear conditioning prevented by blocking NMDA receptors in amygdala Nature 388 1997 471 474 (Pubitemid 27328924)
19. L.E. Gonzalez, N. Andrews, and S.E. File 5-HT1A and benzodiazepine receptors in the basolateral amygdala modulate anxiety in the social interaction test, but not in the elevated plus-maze Brain Res 732 1996 145 153 (Pubitemid 26305299)
20. L. Groenink, R.J. Joordens, T.H. Hijzen, A. Dirks, and B. Olivier Infusion of flesinoxan into the amygdala blocks the fear-potentiated startle Neuroreport 11 2000 2285 2288 (Pubitemid 30485577)
21. B.H. Harvey, C. Naciti, L. Brand, and D.J. Stein Serotonin and stress: protective or malevolent actions in the biobehavioral response to repeated trauma? Ann N Y Acad Sci 1032 2004 267 272 (Pubitemid 40298490)
22. J.A. Harvey Role of the serotonin 5-HT(2A) receptor in learning Learn Mem 10 2003 355 362 (Pubitemid 37266680)
23. C. Heim, and C.B. Nemeroff The role of childhood trauma in the neuroiology of mood and anxiety disorders: precilincal and clinical studies Biol Psychiatry 49 2001 1023 1039 (Pubitemid 32595461)
24. S. Heinrichs, E. Pich, K.A. Miczek, K. Britton, and G. Koob Corticotropin-releasing factor antagonist redues emotionality in socially defeated rats via direct neurotropic action Brain Res 58 1992 190 197
25. I. Hindmarch, J. Schillingford, J.S. Kerr, and J.M. Hesselink The comparative psychopharmacology of 5-HT1A agonists S.M. Stahl, Serotonin 1A Receptors in Depression and Anxiety 1992 Raven Press New York 109 117
26. D. Hoyer, J.P. Hannon, and G.R. Martin Molecular, pharmacological and functional diversity of 5-HT receptors Pharmacol Biochem Behav 71 2002 533 554 (Pubitemid 34219205)
27. K.L. Huhman, T.O. Moore, E.H. Mougey, and J.L. Meyerhoff Hormonal responses to fighting in hamsters: separation of physical and psychological causes Physiol Behav 51 1992 1083 1086
28. A.M. Jasnow, M.A. Cooper, and K.L. Huhman N-methyl-D-aspartate receptors in the amygdala are necessary for the acquisition and expression of conditioned defeat Neuroscience 123 2004 625 634 (Pubitemid 38045401)
29. A.M. Jasnow, C. Shi, J.E. Israel, M. Davis, and K.L. Huhman Memory of social defeat is facilitated by cAMP response element-binding protein overexpression in the amygdala Behav Neurosci 119 2005 1125 1130 (Pubitemid 41377263)
30. X. Jiang, G. Xing, C. Yang, A. Verma, L. Zhang, and H. Li Stress impairs 5-HT2A receptor-mediated serotonergic facilitation of GABA release in juvenile rat basolateral amygdala Neuropsychopharmacology 34 2009 410 423
31. S. Josselyn, C. Shi, W. Carlezon Jr., R.L. Neve, E.J. Nestler, and M. Davis Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala J Neurosci 21 2001 2404 2412 (Pubitemid 32240537)
32. A. Keeney, D. Jessop, M. Harbuz, C.A. Marsden, S. Hogg, and R. Blackburn-Munro Differential effects of acute and chronic social defeat stress on hypothalamic-pituitary-adrenal axis function and hippocampal serotonin release in mice J Neuroendocrinol 18 2006 330 338
33. J. Kehr, X.J. Hu, T. Yoshitake, F.H. Wang, P. Osborne, and C. Stenfors The selective 5-HT(1A) receptor antagonist NAD-299 increases acetylcholine release but not extracellular glutamate levels in the frontal cortex and hippocampus of awake rat Eur Neuropsychopharmacol 20 2010 487 500
34. K.S. Kendler, L.M. Karkowski, and C.A. Prescott Causal relationship between stressful life events and the onset of major depression Am J Psychiatry 156 1999 837 841 (Pubitemid 29260336)
35. H.K. Kia, M.C. Miquel, M.J. Brisorgueil, G. Daval, M. Riad, S. El Mestikawy, M. Hamon, and D. Verge Immunocytochemical localization of serotonin1A receptors in the rat central nervous system J Comp Neurol 365 1996 289 305
36. J.M. Koolhaas, S.F. De Boer, A.J. De Rutter, P. Meerlo, and A. Sgoifo Social stress in rats and mice Acta Physiol Scand Suppl 640 1997 69 72 (Pubitemid 27496284)
37. V. Krishnan, M.-H. Han, D.L. Graham, O. Berton, W. Renthal, and S.J. Russo Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions Cell 131 2007 391 404 (Pubitemid 47576141)
38. C.-J. Kuo, H.-S. Tang, C.-J. Tsay, W.-H. Hu, and C.-C. Chen Prevalence of psychiatric disorders among bereaved survivors of a disastrous earthquake in Taiwan Psychiatr Serv 54 2003 249 251 (Pubitemid 36752859)
39. H. Kusserow, B. Davies, H. Hortnagl, V. Ingo, T. Stroh, and B. Bert Reduced anxiety-related behaviour in transgenic mice overexpression serotonin(1A) receptors Brain Res Molec Brain Res 129 2004 104 116 (Pubitemid 39304254)
40. R. Lanzenberger, M. Mitterhauser, C. Spindelegger, W. Wadsak, N. Klein, and L.K. Mien Reduced serotonin-1A receptor binding in social anxiety disorder Biol Psychiatry 61 2007 1081 1089 (Pubitemid 46551966)
41. R. Lanzenberger, W. Wadsak, C. Spindelegger, M. Mitterhauser, E. Akimova, and L. Mien Cortisol plasma levels in social anxiety disorder patients correlate with serotonin-1A receptor binding in limbic brain regions Int J Neuropsychopharmacol 13 2010 1129 1143
42. K. Lesch Mouse anxiety: the power of knockout Pharmacogenomics J 1 2001 187 192 (Pubitemid 33756658)
43. X. Li, T. Inoue, T. Abekawa, S. Weng, S. Nakagawa, and T. Izumi 5-HT1A receptor agonist affects fear conditioning through stimulations of the postsynaptic 5-HT1A receptors in the hippocampus and amygdala Eur J Pharmacol 532 2006 74 80
44. N. Madjid, E.E. Tottie, M. Luttgen, B. Meister, J. Sandin, and A. Kuzmin 5-Hydroxytryptamine 1A receptor blockade facilitates aversive learning in mice: interactions with cholinergic and glutamatergic mechanisms J Pharmacol Exp Ther 316 2006 581 591 (Pubitemid 43130984)
45. C.A. Markham, S.L. Taylor, and K.L. Huhman Role of amygdala and hippocampus in the neural circuit subserving conditioned defeat in Syrian hamsters Learn Mem 17 2010 109 116
46. C.M. Markham, and K.L. Huhman Is the medial amygdala part of the neural circuit modulating conditioned defeat in Syrian hamsters? Learn Mem 15 2008 6 12 (Pubitemid 351171600)
47. K.R. Melia, and M. Davis Effects of septal lesions on fear-potentiated startle, and on the anxiolytic effects of buspirone and diazepam Physiol Behav 49 1991 603 611
48. I. Misane, C. Johansson, and S.O. Ogren Analysis of the 5-HT1A receptor involvement in passive avoidance in the rat Br J Pharmacol 125 1998 499 509 (Pubitemid 28451488)
49. L.P. Morin, and R.I. Wood A Stereotaxic Atlas of the Golden Hamster Brain 2001 Academic Press San Diego
50. J. Mos, A. Van Hest, M. Van Drimmelen, A.H. Herremans, and B. Olivier The putative 5-HT1A receptor antagonist DU125530 blocks the discriminative stimulus of the 5-HT1A receptor agonist flesinoxan in pigeons Eur J Pharmacol 325 1997 145 153 (Pubitemid 27199563)
51. A. Neumeister, E. Bain, A.C. Nugent, R.E. Carson, O. Bonne, and D.A. Luckenbaugh Reduced serotonin type 1A receptor binding in panic disorder J Neurosci 24 2004 589 591 (Pubitemid 38166482)
52. R.L. Nunes-de-Souza, A. Canto-de-Souza, and R.J. Rodgers Effects of intra-hippocampal infusion of WAY-100635 on plus-maze behavior in mice. Influence of site of injection and prior test experience Brain Res 927 2002 87 96 (Pubitemid 34114052)
53. S.O. Ogren, T.M. Eriksson, E. Elvander-Tottie, C. D'Addario, J.C. Ekstrom, and P. Svenningsson The role of 5-HT1A receptors in learning and memory Behav Brain Res 195 2008 54 77
54. A. Pazos, and J. Palacios Quantitative autoradiographic mapping of serotonin receptors in the rat brain. I. Serotonin-1 Receptors Brain Res 364 1985 205 230 (Pubitemid 16241111)
55. R.L. Pobbe, and H.J. Zangrossi 5-HT(1A) and 5-HT(2A) receptors in the rat dorsal periaqueductal gray mediate the antipanic-like effect induced by the stimulation of serotonergic neurons in the dorsal raphe nucleus Psychopharmacology (Berl) 183 2005 314 321 (Pubitemid 41660417)
56. E.A. Rabiner, C. Messa, P.A. Sarget, K. Husted-Kjaer, A. Montgomery, and A.D. Lawrence A database of [(11C)]WAY-100635 binding to 5-HT(1A) recpetors in normal male volunteers: normative data and relationship to methodological, dmeographic, physiological, and behavioral variables Neuroimage 15 2002 620 632 (Pubitemid 34852530)
57. S. Ramboz, R. Oosting, D.A. Amara, H.F. Kung, P. Blier, and M. Mendelsohn Serotonin receptor 1A knockout: an animal model of anxiety-related disorder Proc Natl Acad Sci USA 95 1998 14476 14481 (Pubitemid 28549392)
58. V.B. Risbrough, J.D. Brodkin, and M.A. Geyer GABA-A and 5-HT1A receptor agonists block expression of fear-potentiated startle in mice Neuropsychopharmacology 28 2003 654 663
59. V.B. Risbrough, and M.B. Stein Role of corticotropin releasing factor in anxiety disorders: a translational research perspective Horm Behav 50 2006 550 561 (Pubitemid 44307112)
60. S.M. Rodrigues, G. Schafe, and J.E. LeDoux Intra-amygdala blockade of the NR2B subunit of the NMDA receptor disrupts the acquisition but not the expression of fear conditioning J Neurosci 21 2001 6889 6896 (Pubitemid 32781131)
61. J. Savitz, I. Lucki, and W.C. Drevets 5-HT(1A) receptor function in major depressive disorder Prog Neurobiol 88 2009 17 31
62. G. Schafe, and J.E. LeDoux Memory consolidation of auditory pavlovian fear conditioning requires protein synthesis and protein kinase A in the amygdala J Neurosci 20 2000 RC96
63. P. Schoeffter, and D. Hoyer Centrally acting hypotensive agents with affinity for 5-HT1A binding sites inhibit forskolin-sitimulated adenylate cyclase activity in calf hippocampus Br J Pharmacol 95 1988 975 985 (Pubitemid 18266277)
64. T. Sharp, S.R. Bramwell, and D.G. Grahame-Smith 5-HT1 agonists reduce 5-hydroxytryptamine release in rat hippocampus in vivo as determined by brain microdialysis Br J Pharmacol 96 1989 283 290 (Pubitemid 19045101)
65. R.M. Sibug, J.C. Compaan, O.C. Meijer, J. Van der Gugten, B. Olivier, and E.R. de Kloet Effects of flesinoxan on corticosteroid receptor expression in the rat hippocampus Eur J Pharmacol 2000 2000 111 119
66. S.C.E. Sporton, S.L. Shepheard, D. Jordan, and A.G. Ramage Microinjections of 5-HT1A agonists into the dorsal motor vagal nucleus produce a bradycardia in the atenolol-pretreated anaesthetized rat Br J Pharmacol 104 1991 466 470
67. O. Stiedl, I. Misane, J. Spiess, and S.O. Ogren Involvement of 5-HT1A receptors in classical fear conditioning in C57BL/6J mice J Neurosci 20 2000 8515 8527
68. P. Strong, B. Greenwood, and M. Fleshner The effects of the selective 5-HT2C receptor antagonist SB 242084 on learned helplessness in male Fischer 344 rats Psychopharmacology (Berl) 203 2009 665 675
69. Y.P. Tang, E. Shimizu, G.R. Dube, C. Rampon, G.A. Kerchner, and M. Zhou Genetic enhancement of learning and memory in mice Nature 401 1999 63 69
70. J. Tauscher, R.M. Bagby, M. Javanmard, B.K. Christensen, S. Kasper, and S. Kapur Inverse relationship between serotonin 5-HT(1A) receptor binding and anxiety: A [(11)C]WAY-100635 PET investigation in healthly volunteers Am J Psychiatry 158 2001 1326 1328 (Pubitemid 32717713)
71. J. Traber, and T. Glaser 5-HT1a receptor-related anxiolytics Trends Pharmacol Sci 8 1987 432 437
72. E. Vermetten, and J.D. Bremner Circuits and systems in stress. II. Applications to neurobiology and treatment in posttraumatic stress disorder Depress Anxiety 16 2002 14 38 (Pubitemid 34977121)
73. W.V. Vieweg, D.A. Julius, A. Fernandez, M. Beatty-Brooks, J.M. Hettema, and A.K. Pandurangi Posttraumatic stress disorder: clinical features, pathophysiology, and treatment Am J Med 119 2006 383 390
74. J. Youn, I. Misane, T.M. Eriksson, M.J. Millan, S.O. Ogren, and M. Verhage Bidirectional modulation of classical fear conditioning in mice by 5-HT1A receptor ligands with contrasting intrinsic activities Neuropharmacology 57 2009 567 576
75. H. Zangrossi Jr., M.B. Viana, and F.G. Graeff Anxiolytic effect of intra-amygdala injection of midazolam and 8-hydroxy-2-(di-n-propylamino)tetralin in the elevated T-maze Eur J Pharmacol 369 1999 267 270 (Pubitemid 29155290)
76. J. Zhang, X.-Y. Huang, M.-L. Ye, C.-X. Luo, H.-Y. Wu, and Y. Hu Neuronal nitric oxide synthase alteration accounts for the role of 5-HT1A receptor in modulating anxiety-related behaviors J Neurosci 30 2010 2433 2441