Short- and Long-Term Functional Consequences of Fluoxetine Exposure During Adolescence in Male Rats

Biological Psychiatry

Volumn 67, Issue 11, 2010, Pages 1057-1066

  Iñiguez, Sergio D ^a   Warren, Brandon L ^a   Bolaños Guzmán, Carlos A ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Adolescence; antidepressant; anxiety; depression; fluoxetine; rat; sexual behavior

Indexed keywords

FLUOXETINE; SUCROSE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AVERSION; CONTROLLED STUDY; COPULATION; DRUG EXPOSURE; FORCED SWIMMING TEST; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SEXUAL BEHAVIOR; STIMULUS RESPONSE; STRESS;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; FEEDING BEHAVIOR; FLUOXETINE; MALE; MOTOR ACTIVITY; RATS; RATS, SPRAGUE-DAWLEY; RECOGNITION (PSYCHOLOGY); SEXUAL BEHAVIOR, ANIMAL; TIME;

EID: 77951877848     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2009.12.033     Document Type: Article

References (124)

1. Kapornai K., and Vetro A. Depression in children. Curr Opin Psychiatry 21 (2008) 1-7
2. Birmaher B., Ryan N.D., Williamson D.E., Brent D.A., Kaufman J., Dahl R.E., et al. Childhood and adolescent depression: A review of the past 10 years. Part I. J Am Acad Child Adolesc Psychiatry 35 (1996) 1427-1439
3. Weissman M.M., Wolk S., Goldstein R.B., Moreau D., Adams P., Greenwald S., et al. Depressed adolescents grown up. JAMA 281 (1999) 1707-1713
4. Pfeffer C.R. Diagnosis of childhood and adolescent suicidal behavior: Unmet needs for suicide prevention. Biol Psychiatry 49 (2001) 1055-1061
5. Rihmer Z. Suicide risk in mood disorders. Curr Opin Psychiatry 20 (2007) 17-22
6. Kovacs M. Presentation and course of major depressive disorder during childhood and later years of the life span. J Am Acad Child Adolesc Psychiatry 35 (1996) 705-715
7. Patten C.A., Choi W.S., Vickers K.S., and Pierce J.P. Persistence of depressive symptoms in adolescents. Neuropsychopharmacology 25 (2001) S89-S91
8. Harrison P.J. The neuropathology of primary mood disorder. Brain 125 (2002) 1428-1449
9. Rohde P., Lewinsohn P.M., and Seeley J.R. Are adolescents changed by an episode of major depression?. J Am Acad Child Adolesc Psychiatry 33 (1994) 1289-1298
10. Andersen S.L., and Teicher M.H. Stress, sensitive periods and maturational events in adolescent depression. Trends Neurosci 31 (2008) 183-191
11. Safer D.J. Should selective serotonin reuptake inhibitors be prescribed for children with major depressive and anxiety disorders?. Pediatrics 118 (2006) 1248-1251
12. Vaswani M., Linda F.K., and Ramesh S. Role of selective serotonin reuptake inhibitors in psychiatric disorders: A comprehensive review. Prog Neuropsychopharmacol Biol Psychiatry 27 (2003) 85-102
13. Pliszka S.R. The use of psychostimulants in the pediatric patient. Pediatr Clin North Am 45 (1998) 1085-1098
14. Emslie G.J., Mayes T.L., and Hughes C.W. Depression: Recent developments and innovative treatments. Psychiatr Clin North Am 23 (2000) 813-835
15. Emslie G.J., and Mayes T.L. Mood disorders in children and adolescents: Psychopharmacological treatment. Biol Psychiatry 49 (2001) 1082-1090
16. Coyle J.T., Pine D.S., Charney D.S., Lewis L., Nemeroff C.B., Carlson G.A., et al. Depression and bipolar support alliance consensus statement on the unmet needs in diagnosis and treatment of mood disorders in children and adolescents. J Am Acad Child Adolesc Psychiatry 42 (2003) 1494-1503
17. Zito J.M., Safer D.J., DosReis S., Gardner J.F., Soeken K., Boles M., et al. Rising prevalence of antidepressants among US youths. Pediatrics 109 (2002) 721-727
18. Birmaher B. Should we use antidepressant medications for children and adolescents with depressive disorders?. Psychopharmacol Bull 34 (1998) 35-39
19. Kratochvil C.J., Vitiello B., Walkup J., Emslie G., Waslick B.D., Weller E.B., et al. Selective serotonin reuptake inhibitors in pediatric depression: Is the balance between benefits and risks favorable?. J Child Adolesc Psychopharmacol 16 (2006) 11-24
20. Coyle J.T. Psychotropic drug use in very young children. JAMA 283 (2000) 1059-1060
21. Zito J.M., Tobi H., de Jong-van den Berg L.T., Fegert J.M., Safer D.J., Janhsen K., et al. Antidepressant prevalence for youths: A multi-national comparison. Pharmacoepidemiol Drug Saf 15 (2006) 793-798
22. de Montigny C., and Blier P. Effects of antidepressant treatments on 5-HT neurotransmission: Electrophysiological and clinical studies. Adv Biochem Psychopharmacol 39 (1984) 223-239
23. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., and Monteggia L.M. Neurobiology of depression. Neuron 34 (2002) 13-25
24. Blakemore S.J., and Choudhury S. Brain development during puberty: State of the science. Dev Sci 9 (2006) 11-14
25. Azmitia E.C. Serotonin and brain: Evolution, neuroplasticity, and homeostasis. Int Rev Neurobiol 77 (2007) 31-56
26. Whitaker-Azmitia P.M. Behavioral and cellular consequences of increasing serotonergic activity during brain development: A role in autism?. Int J Dev Neurosci 23 (2005) 75-83
27. Borue X., Chen J., and Condron B.G. Developmental effects of SSRIs: Lessons learned from animal studies. Int J Dev Neurosci 25 (2007) 341-347
28. Molliver M.E. Serotonergic neuronal systems: What their anatomic organization tells us about function. J Clin Psychopharmacol 7 (1987) 3S-23S
29. Ansorge M.S., Zhou M., Lira A., Hen R., and Gingrich J.A. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 306 (2004) 879-881
30. Cools R., Roberts A.C., and Robbins T.W. Serotoninergic regulation of emotional and behavioural control processes. Trends Cogn Sci 12 (2008) 31-40
31. Harmer C.J., Bhagwagar Z., Perrett D.I., Vollm B.A., Cowen P.J., and Goodwin G.M. Acute SSRI administration affects the processing of social cues in healthy volunteers. Neuropsychopharmacology 28 (2003) 148-152
32. Ansorge M.S., Morelli E., and Gingrich J.A. Inhibition of serotonin but not norepinephrine transport during development produces delayed, persistent perturbations of emotional behaviors in mice. J Neurosci 28 (2008) 199-207
33. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24 (2000) 417-463
34. Seeman P., Bzowej N.H., Guan H.C., Bergeron C., Becker L.E., Reynolds G.P., et al. Human brain dopamine receptors in children and aging adults. Synapse 1 (1987) 399-404
35. Andersen S.L., and Navalta C.P. Altering the course of neurodevelopment: A framework for understanding the enduring effects of psychotropic drugs. Int J Dev Neurosci 22 (2004) 423-440
36. Bhagwagar Z., and Cowen P.J. "It's not over when it's over": Persistent neurobiological abnormalities in recovered depressed patients. Psychol Med 38 (2008) 307-313
37. Duval F., Lebowitz B.D., and Macher J.P. Treatments in depression. Dialogues Clin Neurosci 8 (2006) 191-206
38. Spear L.P., and Brake S.C. Periadolescence: Age-dependent behavior and psychopharmacological responsivity in rats. Dev Psychobiol 16 (1983) 83-109
39. Cryan J.F., Markou A., and Lucki I. Assessing antidepressant activity in rodents: Recent developments and future needs. Trends Pharmacol Sci 23 (2002) 238-245
40. Porsolt R.D. Animal models of depression: Utility for transgenic research. Rev Neurosci 11 (2000) 53-58
41. Wegerer V., Moll G.H., Bagli M., Rothenberger A., Ruther E., and Huether G. Persistently increased density of serotonin transporters in the frontal cortex of rats treated with fluoxetine during early juvenile life. J Child Adolesc Psychopharmacol 9 (1999) 13-24 discussion 25-26
42. Bolaños C.A., Barrot M., Berton O., Wallace-Black D., and Nestler E.J. Methylphenidate treatment during pre- and periadolescence alters behavioral responses to emotional stimuli at adulthood. Biol Psychiatry 54 (2003) 1317-1329
43. Bevins R.A., and Besheer J. Novelty reward as a measure of anhedonia. Neurosci Biobehav Rev 29 (2005) 707-714
44. Friedman A., Frankel M., Flaumenhaft Y., Merenlender A., Pinhasov A., Feder Y., et al. Programmed acute electrical stimulation of ventral tegmental area alleviates depressive-like behavior. Neuropsychopharmacology 34 (2009) 1057-1066
45. Iñiguez S.D., Warren B.L., Parise E.M., Alcantara L.F., Schuh B., Maffeo M.L., et al. Nicotine exposure during adolescence induces a depression-like state in adulthood. Neuropsychopharmacology 34 (2009) 1609-1624
46. Wallace D.L., Han M.H., Graham D.L., Green T.A., Vialou V., Iniguez S.D., et al. CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 12 (2009) 200-209
47. Nestler E.J., and Carlezon Jr. W.A. The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59 (2006) 1151-1159
48. Yadid G., and Friedman A. Dynamics of the dopaminergic system as a key component to the understanding of depression. Prog Brain Res 172 (2008) 265-286
49. Naranjo C.A., Tremblay L.K., and Busto U.E. The role of the brain reward system in depression. Prog Neuropsychopharmacol Biol Psychiatry 25 (2001) 781-823
50. Feder A., Nestler E.J., and Charney D.S. Psychobiology and molecular genetics of resilience. Nat Rev Neurosci 10 (2009) 446-457
51. aan het Rot M., Mathew S.J., and Charney D.S. Neurobiological mechanisms in major depressive disorder. CMAJ 180 (2009) 305-313
52. Kelley A.E., and Berridge K.C. The neuroscience of natural rewards: Relevance to addictive drugs. J Neurosci 22 (2002) 3306-3311
53. Simansky K., and Eberle-Wang K. Serotonergic mechanisms and ingestion: Pharmacological facts and physiological promises. Appetite 21 (1993) 220
54. Halford J.C., Harrold J.A., Lawton C.L., and Blundell J.E. Serotonin (5-HT) drugs: Effects on appetite expression and use for the treatment of obesity. Curr Drug Targets 6 (2005) 201-213
55. Halford J.C., and Blundell J.E. Pharmacology of appetite suppression. Prog Drug Res 54 (2000) 25-58
56. Popa D., Lena C., Alexandre C., and Adrien J. Lasting syndrome of depression produced by reduction in serotonin uptake during postnatal development: Evidence from sleep, stress, and behavior. J Neurosci 28 (2008) 3546-3554
57. Asin K.E., Davis J.D., and Bednarz L. Differential effects of serotonergic and catecholaminergic drugs on ingestive behavior. Psychopharmacology (Berl) 109 (1992) 415-421
58. Besheer J., and Bevins R.A. The role of environmental familiarization in novel-object preference. Behav Processes 50 (2000) 19-29
59. Hughes R.N. Neotic preferences in laboratory rodents: Issues, assessment and substrates. Neurosci Biobehav Rev 31 (2007) 441-464
60. Doremus-Fitzwater TL, Varlinskaya EI, Spear LP (2009): Motivational systems in adolescence: Possible implications for age differences in substance abuse and other risk-taking behaviors [published online ahead of print September 16]. Brain Cogn.
61. Hajnal A., and Norgren R. Accumbens dopamine mechanisms in sucrose intake. Brain Res 904 (2001) 76-84
62. Wallace D.L., Vialou V., Rios L., Carle-Florence T.L., Chakravarty S., Kumar A., et al. The influence of DeltaFosB in the nucleus accumbens on natural reward-related behavior. J Neurosci 28 (2008) 10272-10277
63. Berlyne D.E. The arousal and satiation of perceptual curiosity in the rat. J Comp Physiol Psychol 48 (1955) 238-246
64. Klebaur J.E., and Bardo M.T. The effects of anxiolytic drugs on novelty-induced place preference. Behav Brain Res 101 (1999) 51-57
65. Shimura T., Kamada Y., and Yamamoto T. Ventral tegmental lesions reduce overconsumption of normally preferred taste fluid in rats. Behav Brain Res 134 (2002) 123-130
66. Wise R.A. Role of brain dopamine in food reward and reinforcement. Philos Trans R Soc Lond B Biol Sci 361 (2006) 1149-1158
67. Wise R.A. Dopamine and food reward: Back to the elements. Am J Physiol Regul Integr Comp Physiol 286 (2004) R13
68. Lee K., and Kornetsky C. Acute and chronic fluoxetine treatment decreases the sensitivity of rats to rewarding brain stimulation. Pharmacol Biochem Behav 60 (1998) 539-544
69. Katz R.J., and Carroll B.J. Intracranial reward after Lilly 110140 (fluoxetine HCl): Evidence for an inhibitory role for serotonin. Psychopharmacology (Berl) 51 (1977) 189-193
70. Konkle A.T., and Bielajew C. Feeding and reward interactions from chronic paroxetine treatment. Pharmacol Biochem Behav 63 (1999) 435-440
71. Redgrave P., and Horrell R.I. Potentiation of central reward by localised perfusion of acetylcholine and 5-hydroxytryptamine. Nature 262 (1976) 305-307
72. Matthews K., Baldo B.A., Markou A., Lown O., Overstreet D.H., and Koob G.F. Rewarding electrical brain stimulation: Similar thresholds for Flinders Sensitive Line Hypercholinergic and Flinders Resistant Line Hypocholinergic rats. Physiol Behav 59 (1996) 1155-1162
73. Qi X., Lin W., Li J., Li H., Wang W., Wang D., and Sun M. Fluoxetine increases the activity of the ERK-CREB signal system and alleviates the depressive-like behavior in rats exposed to chronic forced swim stress. Neurobiol Dis 31 (2008) 278-285
74. Collu M., Poggiu A.S., and Serra G. Antidepressants sensitize the dopamine mesolimbic system mediating reward. Behav Pharamcol 7 suppl 1 (1996) 18
75. Collu M., Poggiu A.S., Pani L., and Serra G. Fluoxetine-induced conditioned place preference: A preliminary study. Synapse 25 (1997) 309-311
76. Subhan F., Deslandes P.N., Pache D.M., and Sewell R.D. Do antidepressants affect motivation in conditioned place preference?. Eur J Pharmacol 408 (2000) 257-263
77. Sekine Y., Suzuki K., Ramachandran P.V., Blackburn T.P., and Ashby Jr. C.R. Acute and repeated administration of fluoxetine, citalopram, and paroxetine significantly alters the activity of midbrain dopamine neurons in rats: An in vivo electrophysiological study. Synapse 61 (2007) 72-77
78. Serra G., Collu M., D'Aquila P.S., and Gessa G.L. Role of the mesolimbic dopamine system in the mechanism of action of antidepressants. Pharmacol Toxicol 71 suppl 1 (1992) 72-85
79. Bolaños C.A., Trksak G.H., Cohen O.S., and Jackson D. Differential serotonergic inhibition of in vitro striatal [3H]acetylcholine release in prenatally cocaine-exposed male and female rats. Prog Neuropsychopharmacol Biol Psychiatry 26 (2002) 1339-1348
80. Bolaños C.A., Trksak G.H., Glatt S.J., and Jackson D. Prenatal cocaine exposure increases serotonergic inhibition of electrically evoked acetylcholine release from rat striatal slices at adulthood. Synapse 36 (2000) 1-11
81. Deslandes P.N., Pache D.M., Buckland P., and Sewell R.D. Morphine, cocaine and antidepressant induced motivational activity and midbrain dopaminergic neurotransmission. Eur J Pharmacol 453 (2002) 223-229
82. Nomikos G.G., Damsma G., Wenkstern D., and Fibiger H.C. Chronic desipramine enhances amphetamine-induced increases in interstitial concentrations of dopamine in the nucleus accumbens. Eur J Pharmacol 195 (1991) 63-73
83. Ohl F. Testing for anxiety. Clin Neurosci Res 3 (2003) 233-238
84. Kabbaj M., Devine D.P., Savage V.R., and Akil H. Neurobiological correlates of individual differences in novelty-seeking behavior in the rat: Differential expression of stress-related molecules. J Neurosci 20 (2000) 6983-6988
85. Belzung C., El Hage W., Moindrot N., and Griebel G. Behavioral and neurochemical changes following predatory stress in mice. Neuropharmacology 41 (2001) 400-408
86. Hyman S.E. Methylphenidate-induced plasticity: What should we be looking for?. Biol Psychiatry 54 (2003) 1310-1311
87. Norcross M., Mathur P., Enoch A.J., Karlsson R.M., Brigman J.L., Cameron H.A., et al. Effects of adolescent fluoxetine treatment on fear-, anxiety- or stress-related behaviors in C57BL/6J or BALB/cJ mice. Psychopharmacology (Berl) 200 (2008) 413-424
88. Karpova N.N., Lindholm J., Pruunsild P., Timmusk T., and Castren E. Long-lasting behavioural and molecular alterations induced by early postnatal fluoxetine exposure are restored by chronic fluoxetine treatment in adult mice. Eur Neuropsychopharmacol 19 (2009) 97-108
89. den Boer J.A., Westenberg H.G., Kamerbeek W.D., Verhoeven W.M., and Kahn R.S. Effect of serotonin uptake inhibitors in anxiety disorders; a double-blind comparison of clomipramine and fluvoxamine. Int Clin Psychopharmacol 2 (1987) 21-32
90. Papp L.A., Sinha S.S., Martinez J.M., Coplan J.D., Amchin J., and Gorman J.M. Low-dose venlafaxine treatment in panic disorder. Psychopharmacol Bull 34 (1998) 207-209
91. Nutt D.J., Glue P., and Lawson C. The neurochemistry of anxiety: An update. Prog Neuropsychopharmacol Biol Psychiatry 14 (1990) 737-752
92. 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
93. Belzung C., Le Guisquet A.M., Barreau S., and Calatayud F. An investigation of the mechanisms responsible for acute fluoxetine-induced anxiogenic-like effects in mice. Behav Pharmacol 12 (2001) 151-162
94. Drapier D., Bentue-Ferrer D., Laviolle B., Millet B., Allain H., Bourin M., et al. Effects of acute fluoxetine, paroxetine and desipramine on rats tested on the elevated plus-maze. Behav Brain Res 176 (2007) 202-209
95. Silva R.C., and Brandao M.L. Acute and chronic effects of gepirone and fluoxetine in rats tested in the elevated plus-maze: An ethological analysis. Pharmacol Biochem Behav 65 (2000) 209-216
96. To C.T., Anheuer Z.E., and Bagdy G. Effects of acute and chronic fluoxetine treatment of CRH-induced anxiety. Neuroreport 10 (1999) 553-555
97. Bolaños C.A., Willey M.D., Maffeo M.L., Powers K.D., Kinka D.W., Grausam K.B., et al. Antidepressant treatment can normalize adult behavioral deficits induced by early-life exposure to methylphenidate. Biol Psychiatry 63 (2008) 309-316
98. Britton D.R., and Britton K.T. A sensitive open field measure of anxiolytic drug activity. Pharmacol Biochem Behav 15 (1981) 577-582
99. McCormick CM, Mathews IZ, Thomas C, Waters P (2009): Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models [published online ahead of print July 17]. Brain Cogn.
100. Ramos A., Mellerin Y., Mormede P., and Chaouloff F. A genetic and multifactorial analysis of anxiety-related behaviours in Lewis and SHR intercrosses. Behav Brain Res 96 (1998) 195-205
101. Ramos A., and Mormede P. Stress and emotionality: A multidimensional and genetic approach. Neurosci Biobehav Rev 22 (1998) 33-57
102. Archer J. Tests for emotionality in rats and mice: A review. Anim Behav 21 (1973) 205-235
103. Ramos A. Animal models of anxiety: Do I need multiple tests?. Trends Pharmacol Sci 29 (2008) 493-498
104. Porsolt R.D., Le Pichon M., and Jalfre M. Depression: A new animal model sensitive to antidepressant treatments. Nature 266 (1977) 730-732
105. Lucki I. The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behav Pharmacol 8 (1997) 523-532
106. Hefner K., and Holmes A. Ontogeny of fear-, anxiety- and depression-related behavior across adolescence in C57BL/6J mice. Behav Brain Res 176 (2007) 210-215
107. Oh J.E., Zupan B., Gross S., and Toth M. Paradoxical anxiogenic response of juvenile mice to fluoxetine. Neuropsychopharmacology 34 (2009) 2197-2207
108. de Jong T.R., Snaphaan L.J., Pattij T., Veening J.G., Waldinger M.D., Cools A.R., et al. Effects of chronic treatment with fluvoxamine and paroxetine during adolescence on serotonin-related behavior in adult male rats. Eur Neuropsychopharmacol 16 (2006) 39-48
109. Bolaños C.A., and Nestler E.J. Neurotrophic mechanisms in drug addiction. Neuromolecular Med 5 (2004) 69-83
110. Carlezon Jr. W.A., Duman R.S., and Nestler E.J. The many faces of CREB. Trends Neurosci 28 (2005) 436-445
111. Duman R.S., and Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 59 (2006) 1116-1127
112. Krishnan V., and Nestler E.J. The molecular neurobiology of depression. Nature 455 (2008) 894-902
113. Carlezon Jr. W.A., and Konradi C. Understanding the neurobiological consequences of early exposure to psychotropic drugs: Linking behavior with molecules. Neuropharmacology 47 suppl 1 (2004) 47-60
114. Adriani W., and Laviola G. Windows of vulnerability to psychopathology and therapeutic strategy in the adolescent rodent model. Behav Pharmacol 15 (2004) 341-352
115. Wiley M.D., Poveromo L.B., Antapasis J., Herrera C.M., and Bolanos Guzman C.A. Kappa-opioid system regulates the long-lasting behavioral adaptations induced by early-life exposure to methylphenidate. Neuropsychopharmacology 34 (2009) 1339-1350
116. Sukoff Rizzo S.J., Schechter L.E., and Rosenzweig-Lipson S. A novel approach for predicting antidepressant-induced sexual dysfunction in rats. Psychopharmacology (Berl) 195 (2008) 459-467
117. Cantor J.M., Binik Y.M., and Pfaus J.G. Chronic fluoxetine inhibits sexual behavior in the male rat: Reversal with oxytocin. Psychopharmacology (Berl) 144 (1999) 355-362
118. Ferguson J.M. The effects of antidepressants on sexual functioning in depressed patients: A review. J Clin Psychiatry 62 suppl 3 (2001) 22-34
119. Hull E.M., Muschamp J.W., and Sato S. Dopamine and serotonin: Influences on male sexual behavior. Physiol Behav 83 (2004) 291-307
120. Sukoff Rizzo S.J., Pulicicchio C., Malberg J.E., Andree T.H., Stack G.P., Hughes Z.A., et al. 5-HT1A receptor antagonism reverses and prevents fluoxetine-induced sexual dysfunction in rats. Int J Neuropsychopharmacol 12 (2009) 1045-1053
121. Li Q., Muma N.A., and van de Kar L.D. Chronic fluoxetine induces a gradual desensitization of 5-HT1A receptors: Reductions in hypothalamic and midbrain Gi and G(o) proteins and in neuroendocrine responses to a 5-HT1A agonist. J Pharmacol Exp Ther 279 (1996) 1035-1042
122. Barrot M., Olivier J.D., Perrotti L.I., DiLeone R.J., Berton O., Eisch A.J., et al. CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci U S A 99 (2002) 11435-11440
123. Barrot M., Wallace D.L., Bolanos C.A., Graham D.L., Perrotti L.I., Neve R.L., et al. Regulation of anxiety and initiation of sexual behavior by CREB in the nucleus accumbens. Proc Natl Acad Sci U S A 102 (2005) 8357-8362
124. Sturm V., Lenartz D., Koulousakis A., Treuer H., Herholz K., Klein J.C., et al. The nucleus accumbens: A target for deep brain stimulation in obsessive-compulsive- and anxiety-disorders. J Chem Neuroanat 26 (2003) 293-299