Flibanserin and 8-OH-DPAT implicate serotonin in association between female marmoset monkey sexual behavior and changes in pair-bond quality

Journal of Sexual Medicine

Volumn 9, Issue 3, 2012, Pages 694-707

  Aubert, Yves ^a,b   Gustison, Morgan L ^a,c   Gardner, Lindsey A ^a   Bohl, Michael A ^a   Lange, Jason R ^a   Allers, Kelly A ^d   Sommer, Bernd ^d   Datson, Nicole A ^b   Abbott, David H ^a,e,f  

^a UNIVERSITY OF WISCONSIN   (United States)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF MICHIGAN   (United States)

^d BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^e UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^f UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Affiliative behavior; Female sexual function; Flibanserin; HSDD; Pharmacologic treatment of female sexual dysfunction; Serotonin receptor

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; FLIBANSERIN; SEROTONIN;

ANIMAL EXPERIMENT; ARTICLE; CALLITRICHINAE; CONTROLLED STUDY; FEMALE; GROOMING; MALE; NONHUMAN; OUTCOME ASSESSMENT; PHYSICAL ATTRACTIVENESS; PRIORITY JOURNAL; SEXUAL BEHAVIOR; SEXUAL SELECTION; SOCIAL BEHAVIOR;

EID: 84857641125     PISSN: 17436095     EISSN: 17436109     Source Type: Journal    
DOI: 10.1111/j.1743-6109.2011.02616.x     Document Type: Article

References (73)

1. Clayton AH. The pathophysiology of hypoactive sexual desire disorder in women. Int J Gynaecol Obstet 2010;110:7-11.
2. Pfaus JG. Pathways of sexual desire. J Sex Med 2009;6:1506-33.
3. Clayton AH, Hamilton DV. Female sexual dysfunction. Psychiatr Clin North Am 2010;33:323-38.
4. Rosen RC, Lane RM, Menza M. Effects of SSRIs on sexual function: A critical review. J Clin Psychopharmacol 1999;19:67-85.
5. Barnes NM, Sharp T. A review of central 5-HT receptors and their functions. Neuropharmacology 1999;38:1083-152.
6. Ahlenius S, Fernandez-Guasti A, Hjorth S, Larsson K. Suppression of lordosis behavior by the putative 5-HT receptor agonist 8-OH-DPAT in the rat. Eur J Pharmacol 1986;124:361-3.
7. Uphouse L, Caldarola-Pastuszka M, Montanez S. Intracerebral actions of the 5-HT1A agonists, 8-OH-DPAT and buspirone and of the 5-HT1A partial agonist/antagonist, NAN-190, on female sexual behavior. Neuropharmacology 1992;31:969-81.
8. Maswood N, Caldarola-Pastuszka M, Uphouse L. 5-HT3 receptors in the ventromedial nucleus of the hypothalamus and female sexual behavior. Brain Res 1997;769:13-20.
9. Mendelson SD, Gorzalka BB. A facilitatory role for serotonin in the sexual behavior of the female rat. Pharmacol Biochem Behav 1985;22:1025-33.
10. Borsini F, Giraldo E, Monferini E, Antonini G, Parenti M, Bietti G, Donetti A. BIMT 17, a 5-HT2A receptor antagonist and 5-HT1A receptor full agonist in rat cerebral cortex. Naunyn Schmiedebergs Arch Pharmacol 1995;352:276-282.
11. Borsini F, Ceci A, Bietti G, Conetti A. BIMT 17, a 5-HT1A receptor agonist/5-HT2A receptor antagonist, directly activates postsynaptic 5-HT inhibitory responses in the rat cerebral cortex. Naunyn Schmiedebergs Arch Pharmacol 1995b;352:283-90.
12. Borsini F, Evans K, Jason K, Rohde F, Alexander B, Pollentier S. Pharmacology of flibanserin. CNS Drug Rev 2002;8:117-42.
13. Gelez H, Allers K, Sommer B, Giuliano F. Chronic Flibanserin treatment increases solicitations in the female rat. J Sex Med 2010;7(suppl 3):118.
14. Kennedy S. Flibanserin: Initial evidence of efficacy on sexual dysfunction, in patients with major depressive disorder. J Sex Med 2010;7:3449-59.
15. Stahl SM, Sommer B, Allers KA. Multifunctional pharmacology of flibanserin: Possible mechanism of therapeutic action in hypoactive sexual desire disorder. J Sex Med 2011;8:15-27.
16. Arvidsson LE, Hacksell U, Nilsson JL, Hjorth S, Carlsson A, Lindberg P, Sanchez D, Wikstrom H. 8-Hydroxy-2-(di-n-propylamino)tetralin, a new centrally acting 5-hydroxytryptamine receptor agonist. J Med Chem 1981;24:921-3.
17. Uphouse L, Montanez S, Richards-Hill R, Caldarola-Pastuszka M, Droge M. Effects of the 5-HT1A agonist, 8-OH-DPAT, on sexual behaviors of the proestrous rat. Pharmacol Biochem Behav 1991;39:635-40.
18. Abbott DH, Barnett DK, Colman RJ, Yamamoto ME, Schultz-Darken NJ. Aspects of common marmoset basic biology and life history important for biomedical research. Comp Med 2003;53:339-50.
19. Barnett DK, Bunnell TM, Millar RP, Abbott DH. Gonadotropin-releasing hormone II stimulates female sexual behavior in marmoset monkeys. Endocrinology 2006;147:615-23.
20. Evans S, Poole TB. Long-term changes and maintenance of the pair-bond in common marmosets, Callithrix jacchus jacchus. Folia Primatol 1984;42:33-41.
21. Stevenson MF, Poole TB. An ethogram of the common marmoset (Calithrix jacchus jacchus): General behavioural repertoire. Anim Behav 1976;24:428-51.
22. Hearn JP. Restraining device for small monkeys. Lab Anim 1977;11:261-2.
23. Sharma V, McNeill JH. To scale or not to scale: The principles of dose extrapolation. Br J Pharmacol 2009;157:907-21.
24. Jolly E, Clayton AH, Thorp J, Kimura T, Sand M, Pyke R. Efficacy of flibanserin 100 mg qhs as a potential treatment for hypoactive sexual desire disorder in North American premenopausal women. J Sex Med 2009;6(suppl 5):465.
25. Elliott PJ, Walsh DM, Close SP, Higgins GA, Hayes AG. Behavioural effects of serotonin agonists and antagonists in the rat and marmoset. Neuropharmacology 1990;29:949-56.
26. Johansson CE, Meyerson BJ. The effects of long-term treatment with 8-OH-DPAT on the lordosis response and hypothermia in female rats. Eur J Pharmacol 1991;196:143-7.
27. Saltzman W, Schultz-Darken NJ, Wegner FH, Wittwer DJ, Abbott DH. Suppression of cortisol levels in subordinate female marmosets: Reproductive and social contributions. Horm Behav 1998;33:58-74.
28. Kendrick KM, Dixson AF. The effect of the ovarian cycle on the sexual behaviour of the common marmoset (Callithrix jacchus). Physiol Behav 1983;30:735-42.
29. Kendrick KM, Dixson AF. Effects of oestradiol 17B, progesterone and testosterone upon proceptivity and receptivity in ovariectomized common marmosets (Callithrix jacchus). Physiol Behav 1985;34:123-8.
30. Allers KA, Gelez H, Sommer B, Guiliano F. Activation of the immediate early gene c-fos by acute and repeated treatment with flibanserin. J Sex Med 2010;7(suppl 4):151.
31. Tricklebank MD, Forler C, Fozard JR. The involvement of subtypes of the 5-HT1 receptor and of catecholaminergic systems in the behavioural response to 8-hydroxy-2-(di-n-propylamino)tetralin in the rat. Eur J Pharmacol 1984;106:271-82.
32. Borsini F, Brambilla A, Cesana R, Grippa N. Lack of interaction between flibanserin and antidepressants in inducing serotonergic syndrome in rats. Int J Neuropsychopharmacol 2001;4:9-15.
33. Bland JM, Altman DG. Statistics notes: Transforming data. BMJ 1996;312:770-1.
34. Guptarak J, Sarkar J, Hiegel C, Uphouse L. Role of 5-HT(1A) receptors in fluoxetine-induced lordosis inhibition. Horm Behav 2010;58:290-6.
35. Uphouse L, Caldarola-Pastuszka M, Moore N. Inhibitory effects of the 5-HT1A agonists, 5-hydroxy- and 5-methoxy-(3-di-n-propylamino)chroman, on female lordosis behavior. Neuropharmacology 1993;32:641-51.
36. Uphouse L, Caldarola-Pastuszka M. Female sexual behavior following intracerebral infusion of the 5-HT1A agonist, 8-OH-DPAT, into the medial preoptic area. Brain Res 1993;601:203-8.
37. Uphouse L, Maswood S, Caldarola-Pastuszka M. Agonist activation of 5-HT1A receptors in the median raphé nucleus and female rat lordosis behavior. Brain Res 1994;668:271-5.
38. Johansson CE, Meyerson BJ, Höglund AU. The long-term effects of 8-hydroxy-2-(di-n-propyl-amino)tetralin (8-OH-DPAT) on copulatory and exploratory behaviour in male rats. Eur J Pharmacol 1990;178:1-9.
39. Kannan S, Archunan G. Chemistry of clitoral gland secretions of the laboratory rat: Assessment of behavioural response to identified compounds. J Biosci 2001;26:247-52.
40. Ferris CF, Snowdon CT, King JA, Sullivan JM Jr, Ziegler TE, Olson DP, Schultz-Darken NJ, Tannenbaum PL, Ludwig R, Wu Z, Einspanier A, Vaughan JT, Duong TQ. Activation of neural pathways associated with sexual arousal in non-human primates. J Magn Reson Imaging 2004;19:168-75.
41. Ferreira-Nuño A, Morales-Otal A, Paredes RG, Velázquez-Moctezuma J. Sexual behavior of female rats in a multiple-partner preference test. Horm Behav 2005;47:290-6.
42. Dixson AF, Lunn SF. Post-partum changes in hormones and sexual behaviour in captive groups of marmosets (Callithrix jacchus). Physiol Behav 1987;41:577-83.
43. Ho SS, Chow BK, Yung WH. Serotonin increases the excitability of the hypothalamic paravenricular nucleus magnocellular neurons. Eur J Neurosci 2007;25:2991-3000.
44. Keverne EB, Curley JP. Vasopressin, oxytocin and social behaviour. Curr Opin Neurobiol 2004;14:777-83.
45. de Arruda Camargo GM, de Arruda Camargo LA, Saad WA. Role of serotonergic 5-HT1A and oxytocinergic receptors of the lateral septal area in sodium intake regulation. Behav Brain Res 2010;209:260-6.
46. Pedersen CA, Caldwell JD, Peterson G, Walker CH, Mason GA. Oxytocin activation of maternal behavior in the rat. Ann N Y Acad Sci 1992;652:58-69.
47. Bancroft J, Loftus J, Long JS. Distress about sex: A national survey of women in heterosexual relationships. Arch Sex Behav 2003;32:193-208.
48. Carter CS. Neuroendocrine perspectives on social attachment and love. Psychoneuroendocrinology 1998;23:779-818.
49. Snowdon CT, Ziegler TE, Schultz-Darken NJ, Ferris CF. Social odours, sexual arousal and pairbonding in primates. Philos Trans R Soc Lond B Biol Sci 2006;361:2079-89.
50. Evans S. The pair-bond of the common marmoset, Callithrix jacchus jacchus: An experimental investigation. Anim Behav 1983;31:651-8.
51. Anzenberger G. How stranger encounters of common marmosets (Callithrix jacchus jacchus) are influenced by family members: The quality of behavior. Folia Primatol 1985;45:204-24.
52. Insel TR, Winslow JT. Serotonin and neuropeptides in affiliative behaviors. Biol Psychiatry 1998;44:207-19.
53. Young KA, Gobrogge KL, Liu Y, Wang Z. The neurobiology of pair bonding: Insights from a socially monogamous rodent. Front Neuroendocrinol 2011;32:53-69.
54. Ferris CF. Serotonin diminishes aggression by suppressing the activity of the vasopressin system. Ann N Y Acad Sci 1996;794:98-103.
55. Snowdon CT, Pieper BA, Boe CY, Cronin KA, Kurian AV, Ziegler TE. Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins. Horm Behav 2010;58:614-8.
56. Gerretsen P, Graff-Guerrero A, Menon M, Pollock BG, Kapur S, Vasdev N, Houle S, Mamo D. Is desire for social relationships mediated by the serotonergic system in the prefrontal cortex? An [(18)F]setoperone PET study. Soc Neurosci 2010;5:375-83.
57. Allers KA, Dremencov E, Ceci A, Flik G, Ferger B, Cremers TI, Ittrich C, Sommer B. Acute and repeated flibanserin administration in female rats modulates monoamines differentially across brain areas: A microdialysis study. J Sex Med 2010;7:1757-67.
58. Ferger B, Shimasaki M, Ceci A. Flibanserin, a drug intended for treatment of hypoactive sexual desire disorder in pre-menopausal women, affects spontaneous motor activity and brain neurochemistry in female rats. Naunyn Schmiedebergs Arch Pharmacol 2010;381:573-9.
59. Arnow BA, Millheiser L, Garrett A, Lake Polan M, Glover GH, Hill KR, Lightbody A, Watson C, Banner L, Smart T, Buchanan T, Desmond JE. Women with hypoactive sexual desire disorder compared to normal females: A functional magnetic resonance imaging study. Neuroscience 2009;158:484-502.
60. Holstege G, Willemsen A, Beers C, Lont E, Schultz WW, Jansen M, Dierck R. Differences in brain activity in premenopausal women with hyopoactive sexual desire disorder (HSDD) compared to women without sexual dysfunction. J Sex Med 2009;6(suppl 5):407.
61. Laumann EO, Paik A, Rosen RC. Sexual dysfunction in the United States: Prevalence and predictors. JAMA 1999;28:537-44.
62. Pfaff DW. Estrogens and brain function. New York: Springer; 1980.
63. Wallen K, Zehr JL. Hormones and history: The evolution and development of primate female sexuality. J Sex Res 2004;41:101-12.
64. Tricklebank MD, Forler C, Middlemiss DN, Fozard JR. Subtypes of the 5-HT receptor mediating the behavioural responses to 5-methoxy-N, N-dimethyltryptamine in the rat. Eur J Pharmacol 1985;117:15-24.
65. Larsson LG, Rényi L, Ross SB, Svensson B, Angeby-Möller K. Different effects on the responses of functional pre- and postsynaptic 5-HT1A receptors by repeated treatment of rats with the 5-HT1A receptor agonist 8-OH-DPAT. Neuropharmacology 1990;29:85-91.
66. Arnt J, Hyttel J. Facilitation of 8-OH-DPAT-induced forepaw treading of rats by the 5-HT2 agonist DOI. Eur J Pharmacol 1989;161:45-51.
67. Rogóz Z, Skuza G, Legutko B. Repeated co-treatment with fluoxetine and amantadine induces brain-derived neurotrophic factor gene expression in rats. Pharmacol Rep 2008;60:817-26.
68. Dunkley EJ, Isbister GK, Sibbritt D, Dawson AH, Whyte IM. The Hunter Serotonin Toxicity Criteria: Simple and accurate diagnosis decision rules for serotonin toxicity. Q J Med 2003;96:635-42.
69. Isbister GK, Buckley NA. The pathophysiology of serotonin toxicity in animals and humans: Implications for diagnosis and treatment. Clin Neuropharmacol 2005;28:205-14.
70. Hjorth S. Hypothermia in the rat induced by the potent serotonergic agent 8-OH-DPAT. J Neural Transm 1985;61:131-5.
71. Anderson IM, Cowen PJ, Grahame-Smith DG. The effects of gepirone on neuroendocrine function and temperature in humans. Psychopharmacology (Berl) 1990;100:498-503.
72. Brambilla A, Baschirotto A, Grippa N, Borsini F. Effect of flibanserin (BIMT 17), fluoxetine, 8-OH-DPAT and buspirone on serotonin synthesis in rat brain. Eur Neuropsychopharmacol 1999;10:63-7.
73. Bethea CL, Ku NZ, Gundlah C, Streicher JM. Diverse actions of ovarian steroids in the serotonin neural system. Front Neuroendocrinol 2002;23:41-100.