Sociosexual behaviours in cycling, intact female rats (Rattus norvegicus) housed in a seminatural environment

Behaviour

Volumn 151, Issue 8, 2014, Pages 1143-1184

  Chu, Xi ^a   Ågmo, Anders ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

Author keywords

estrus cycle; female preference; fertility; lordosis; sexual behaviour; social behaviour

Indexed keywords

EID: 84905270406     PISSN: 00057959     EISSN: 1568539X     Source Type: Journal    
DOI: 10.1163/1568539X-00003177     Document Type: Article

References (90)

1. Adler, N.T. (1969). Effects of the male's copulatory behavior on successful pregnancy in the female rat.- J. Comp. Physiol. Psychol. 69: 613-622.
2. Ågmo, A. (1997). Male rat sexual behavior. - Brain Res. Protocols 1: 203-209.
3. Ågmo, A. (1999). Sexual motivation. An inquiry into events determining the occurrence of sexual behavior. -Behav. Brain Res. 105: 129-150.
4. Ågmo, A. (2007). Functional and dysfunctional sexual behavior. A synthesis of neuroscience and comparative psychology. - Academic Press, San Diego, CA.
5. Ågmo, A. & Soria, P. (1997). GABAergic drugs and sexual motivation, receptivity and exploratory behaviors in the female rat. -Psychopharmacology 129: 372-381.
6. Albert, D.J., Jonik, R.H. & Walsh, M.L. (1992). Hormone-dependent aggression in male and female rats: experiential, hormonal, and neural foundations. - Neurosci. Biobehav. Rev. 16: 177-192.
7. Araujo, D., Davids, K. & Passos, P. (2007). Ecological validity, representative design, and correspondence between experimental task constraints and behavioral setting: Comment on Rogers, Kadar, and Costall (2005).- Ecol. Psychol. 19: 69-78.
8. Aubele, T., Kaufman, R., Montalmant, F. & Kritzer, M.F. (2008). Effects of gonadectomy and hormone replacement on a spontaneous novel object recognition task in adult male rats. -Horm. Behav. 54: 244-252.
9. Auger, A.P., Moffatt, C.A. & Blaustein, J.D. (1997). Progesterone independent activation of rat brain progestin receptors by reproductive stimuli. - Endocrinology 138: 511-514.
10. Ball, J. (1937). A test for measuring sexual excitability in the female rat. - Comp. Psychol. Monogr. 14: 1-37.
11. Bennett, A.L., Blasberg, M.E. & Blaustein, J.D. (2001). Sensory cues mediating matinginduced potentiation of sexual receptivity in female rats.- Horm. Behav. 40: 77-83.
12. Bennett, A.L., Blasberg, M.E. & Blaustein, J.D. (2002). Mating stimulation required for mating-induced estrous abbreviation in female rats: effects of repeated testing. - Horm. Behav. 42: 206-211.
13. Blandau, R.J., Boling, J.L. & Young, W.C. (1941). The length of heat in the albino rat as determined by the copulatory response.- Anat. Rec. 79: 453-463.
14. Blaustein, J.D. & Erskine, M.S. (2002). Feminine sexual behavior: cellular integration of hormonal and afferent information in the rodent brain.-In: Hormones, brain and behavior, Vol. 1 (Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrbach, S.E. & Rubin, R.T., eds). Academic Press, New York, NY, p. 139-214.
15. Blaustein, J.D., Farrell, S., Ghavami, G., Laroche, J. & Mohan, G. (2009). Non-intromissive mating stimuli are sufficient to enhance sexual behaviors in ovariectomized female rats. -Horm. Behav. 55: 404-411.
16. Boling, J.L. & Blandau, R.J. (1939). The estrogen-progesterone induction of mating responses in the spayed female rat. -Endocrinology 25: 359-364.
17. Brunswik, E. (1955). Representative design and probabilistic theory in a functional psychology.- Psychol. Rev. 62: 193-217.
18. Calhoun, J.B. (1962). The ecology and sociology of the Norway rat. - US Governnment Printing Office, Washington, DC.
19. Conover, W.J. (1999). Practical nonparametric statistics, 3rd edn.- Wiley, New York, NY.
20. Coopersmith, C., Candurra, C. & Erskine, M.S. (1996). Effects of paced mating and intromissive stimulation on feminine sexual behavior and estrus termination in the cycling rat. -J. Comp. Psychol. 110: 176-186.
21. Dewsbury, D.A. (1967). A quantitative description of the behavior of rats during copulation. -Behaviour 29: 154-178.
22. Edwards, D.A., Whalen, R.E. & Nadler, R.D. (1968). Induction of estrus: estrogen-progesterone interactions. - Physiol. Behav. 3: 29.
23. Eliasson, M. & Meyerson, B.J. (1975). Sexual preference in female rats during estrous cycle, pregnancy and lactation. - Physiol. Behav. 14: 705-710.
24. Ellingsen, E. & Ågmo, A. (2004). Sexual incentive motivation and paced sexual behavior in female rats after treatment with drugs modifying dopaminergic neurotransmission. - Pharmacol. Biochem. Behav. 77: 431-445.
25. Erskine, M.S. (1989). Solicitation behavior in the estrous female rat: a review. - Horm. Behav. 23: 473-502.
26. Erskine, M.S. (1992). Pelvic and pudendal nerves influence the display of paced mating behavior in response to estrogen and progesterone in the female rat. - Behav. Neurosci. 106: 690-697.
27. Erskine, M.S. & Baum, M.J. (1982). Effects of paced coital stimulation on termination of estrus and brain indoleamine levels in female rats. - Pharmacol. Biochem. Behav. 17: 857-861.
28. Erskine, M.S., Kornberg, E. & Cherry, J.A. (1989). Paced copulation in rats - effects of intromission frequency and duration on luteal activation and estrus length. - Physiol. Behav. 45: 33-39.
29. Fadem, B.H., Barfield, R.J. & Whalen, R.E. (1979). Dose-response and time-response relationships between progesterone and the display of patterns of receptive and proceptive behavior in the female rat.- Horm. Behav. 13: 40-48.
30. Feder, H.H. (1984). Hormones and sexual behavior. - Annu. Rev. Psychol. 35: 165-200.
31. French, D., Fitzpatrick, D. & Law, O.T. (1972). Operant investigation of mating preferences in female rats.- J. Comp. Physiol. Psychol. 81: 226-232.
32. Frye, C.A. & Walf, A.A. (2004). Estrogen and/or progesterone administered systemically or to the amygdala can have anxiety-reducing, fear-reducing, and pain-reducing effects in ovariectomized rats. -Behav. Neurosci. 118: 306-313.
33. Frye, C.A., Bayon, L.E., Pursnani, N.K. & Purdy, R.H. (1998). The neurosteroids, progesterone and 3α,5α-THP, enhance sexual motivation, receptivity, and proceptivity in female rats.- Brain Res. 808: 72-83.
34. Frye, C.A., Bayon, L.E. & Vongher, J. (2000). Intravenous progesterone elicits a more rapid induction of lordosis in rats than does SKF38393.-Psychobiology 28: 99-109.
35. Frye, C.A., Paris, J.J. & Rhodes, M.E. (2008). Exploratory, anti-anxiety, social, and sexual behaviors of rats in behavioral estrus is attenuated with inhibition of 3α,5α-THP formation in the midbrain ventral tegmental area.- Behav. Brain Res. 193: 269-276.
36. Gaskin, S., Tardif, M., Cole, E., Piterkin, P., Kayello, L. & Mumby, D.G. (2010). Object familiarization and novel-object preference in rats.- Behav. Proc. 83: 61-71.
37. Gentry, R.T. & Wade, G.N. (1976). Sex differences in sensitivity of food intake, body weight, and running-wheel activity to ovarian steroids in rats. - J. Comp. Physiol. Psychol. 90: 747-754.
38. Georgescu, M., Cyr, D. & Pfaus, J.G. (2012). AMPA/kainate receptors in the ventromedial hypothalamus mediate the effects of glutamate on estrus termination in the rat. - Pharmacol. Biochem. Behav. 102: 146-150.
39. Giordano, M., Güemes, M., López-Arias, V. & Paredes, R.G. (2000). Socio-sexual behavior in male rats after lesions of the dorsolateral tegmentum. - Physiol. Behav. 65: 89-94.
40. Gonzalez-Flores, O., Beyer, C., Lima-Hernandez, F.J., Gomora-Arrati, P., Gomez-Camarillo, M.A., Hoffman, K. & Etgen, A.M. (2007). Facilitation of estrous behavior by vaginal cervical stimulation in female rats involves alpha1-adrenergic receptor activation of the nitric oxide pathway. - Behav. Brain Res. 176: 237-243.
41. Hemmingsen, A.M. (1933). Studies on the oestrus-producing hormone (oestrin). - Skand. Arch. Physiol. 65: 97-250.
42. Hlinak, Z. (1993). Social recognition in ovariectomized and estradiol-treated female rats. - Horm. Behav. 27: 159-166.
43. Hlinak, Z. & Madlafousek, J. (1982). Initiation of copulatory behavior in castrated male rats implanted with very small testosterone-filled silastic capsules. - Endokrinologie 79: 35-43.
44. Hlinak, Z., Madlafousek, J. & Mohapelova, A. (1979). Initiation of copulatory activity in castrated male rats injected with critically adjusted doses of testosterone.-Horm. Behav. 13: 9-20.
45. Hori, T., Ide, M. & Miyake, T. (1968). Ovarian estrogen secretion during estrous cycle and under influence of exogenous gonadotropins in rats. -Endocrinol. Jpn. 15: 215-222.
46. Hull, E.M., Meisel, R.L. & Sachs, B.D. (2002). Male sexual behavior.-In: Hormones, brain and behavior, Vol. 1 (Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrbach, S.E. & Rubin, R.T., eds). Academic Press, New York, NY, p. 3-137.
47. Komisaruk, B.R. & Diakow, C. (1973). Lordosis reflex intensity in rats in relation to the estrous cycle, ovariectomy, estrogen administration and mating behavior.-Endocrinology 93: 548-557.
48. Landau, I.T. & Madden, J.E. (1983). Hormonal regulation of female proceptivity and its influence on male sexual preference in rats.- Physiol. Behav. 31: 679-685.
49. Larsson, K., Feder, H.H. & Komisaruk, B.R. (1974). Role of the adrenal glands, repeated matings and monoamines in lordosis behavior of rats. - Pharmacol. Biochem. Behav. 2: 685-692.
50. Latané, B. & Glass, D.C. (1968). Social and nonsocial attraction in rats. - J. Personal. Soc. Psychol. 9: 142-146.
51. Llaneza, D.C. & Frye, C.A. (2009). Progestogens and estrogen influence impulsive burying and avoidant freezing behavior of naturally cycling and ovariectomized rats. - Pharmacol. Biochem. Behav. 93: 337-342.
52. Lodder, J. & Zeilmaker, G.H. (1976). Role of pelvic nerves in post-copulatory abbreviation of behavioral estrus in female rats.- J. Comp. Physiol. Psychol. 90: 925-929.
53. Long, A. & Evans, H.M. (1922). The oestrus cycle of the rat and its associated phenomena. -Memoirs Univ. California 6: 1-148.
54. Macdonald, G.J. (1978). Factors involved in maintenance of pregnancy in the rat: temporal need for estrogen, pituitary prolactin and the ovary.- Biol. Reprod. 19: 817-823.
55. Madlafousek, J. & Hlinak, Z. (1978). Sexual behavior of the female laboratory rat: inventory, patterning, and measurement.-Behaviour 63: 129-174.
56. Madlafousek, J. & Hlinak, Z. (1983). Importance of female's precopulatory behaviour for the primary initiation of male's copulatory behaviour in the laboratory rat. - Behaviour 86: 237-249.
57. Mani, S. (2003). Signalling mechanisms in progesterone-neurotransmitter interactions. - J. Mol. Endocrinol. 30: 127-137.
58. Mani, S. & Portillo, W. (2010). Activation of progestin receptors in female reproductive behavior: interactions with neurotransmitters. - Front. Neuroendocrinol. 31: 157-171.
59. Mani, S.K., Portillo, W. & Reyna, A. (2009). Steroid hormone action in the brain: cross-talk between signalling pathways.- J. Neuroendocrinol. 21: 243-247.
60. Matochik, J.A., White, N.M. & Barfield, R.J. (1992). Variations in scent marking and ultrasonic vocalizations by Long-Evans rats across the estrous cycle. - Physiol. Behav. 51: 783-786.
61. McClintock, M.K. (1984). Group mating in the domestic rat as a context for sexual selection: consequences for the analysis of sexual behavior and neuroendocrine responses. - Adv. Stud. Behav. 14: 1-50.
62. McClintock, M.K. (1987). A functional approach to the behavioral endocrinology of rodents. -In: Psychobiology of reproductive behavior. An evolutionary approach (Crew, D., ed.). Prentice-Hall, Englewood Cliffs, NJ, p. 176-203.
63. McClintock, M.K. & Adler, N.T. (1978). The role of the female during copulation in wild and domestic Norway rats (Rattus norvegicus). - Behaviour 67: 67-96.
64. McClintock, M.K. & Anisko, J.J. (1982). Group mating among Norway rats. I. Sex differences in the pattern and neuroendocrine consequences of copulation.-Anim. Behav. 30: 398-409.
65. McClintock, M.K., Anisko, J.J. & Adler, N.T. (1982). Group mating among Norway rats. II. The social dynamics of copulation: competition, cooperation, and mate choice. - Anim. Behav. 30: 410-425.
66. Paredes, R.G. & Alonso, A. (1997). Sexual behavior regulated (paced) by the female induces conditioned place preference. -Behav. Neurosci. 111: 123-128.
67. Paredes, R.G., Highland, L. & Karam, P. (1993). Socio-sexual behavior in male rats after lesions of the medial preoptic area: evidence for reduced sexual motivation.-Brain Res. 618: 271-276.
68. Petrinovich, L. (1980). Brunswikian behavioral biology. - In: Realizations of Brunswik's representative design (Hammond, K.R. & Wascoe, N.E., eds). Jossey-Bass, San Francisco, CA, p. 85-93.
69. Pfaff, D., Frohlich, J. & Morgan, M. (2002). Hormonal and genetic influences on arousalsexual and otherwise. - Trends Neurosci. 25: 45-50.
70. Pfaff, D.W. (1999). Drive. Neurobiological and molecular mechanisms of sexual motivation. -MIT Press, Cambridge, MA.
71. Pfaus, J.G., Smith, W.J., Byrne, N. & Stephens, G. (2000). Appetitive and consummatory sexual behaviors of female rats in bilevel chambers. II. Patterns of estrus termination following vaginocervical stimulation. -Horm. Behav. 37: 96-107.
72. Rajendren, G., Dudley, C.A. & Moss, R.L. (1990). Role of the vomeronasal organ in the male-induced enhancement of sexual receptivity in female rats. - Neuroendocrinology 52: 368-372.
73. Robitaille, J.A. & Bouvet, J. (1976). Field observations on the social behaviour of the Norway rat, Rattus norvegicus (Berkenhout). -Biol. Behav. 1: 289-308.
74. Rodier, W.I. (1971). Progesterone-estrogen interactions in control of activity-wheel running in the female rat. -J. Comp. Physiol. Psychol. 74: 365-373.
75. Rodier, W.I. & Segal, S. (1977). The effect of progesterone on activity-wheel running of ovariectomized rats. -Horm. Behav. 9: 214-221.
76. Rodriguez-Sierra, J.F., Crowley, W.R. & Komisaruk, B.R. (1975). Vaginal stimulation in rats induces prolonged lordosis responsiveness and sexual receptivity. - J. Comp. Physiol. Psychol. 89: 79-85.
77. Spiteri, T. & Ågmo, A. (2009). Ovarian hormones modulate social recognition in female rats. -Physiol. Behav. 98: 247-250.
78. Spiteri, T., Ogawa, S., Musatov, S., Pfaff, D.W. & Ågmo, A. (2012). The role of the estrogen receptor α in the medial preoptic area in sexual incentive motivation, proceptivity and receptivity, anxiety, and wheel running in female rats.- Behav. Brain Res. 230: 11-20.
79. Steiniger, F. (1950). Beiträge zur Soziologie und sonstigen Biologie der Wanderratte. - Z. Tierpsychol. 7: 356-379.
80. Taylor, G.T. & Weiss, J. (1987). Behavior and fecundity of female rats mated with preferred or non-preferred males.- Anim. Behav. 35: 115-121.
81. Telle, H.J. (1966). Beitrag zur Kenntnis der Verhaltensweise von Ratten, vergleichend dargestellt bei Rattus norvegicus und Rattus rattus. -Z. Angew. Zool. 53: 129-196.
82. Tennent, B.J., Smith, E.R. & Davidson, J.M. (1980). The effects of estrogen and progesterone on female rat proceptive behavior. -Horm. Behav. 14: 65-75.
83. Traslavina, G.A.A. & Franci, C.R. (2011). The CRH-R-1 receptor mediates luteinizing hormone, prolactin, corticosterone and progesterone secretion induced by restraint stress in estrogen-primed rats.- Brain Res. 1421: 11-19.
84. Uchida, K., Kadowaki, M. & Miyake, T. (1969). Ovarian secretion of progesterone and 20α- hydroxypregn-4-en-3-one during rat estrous cycle in chronological relation to pituitary release of luteinizing hormone.- Endocrinol. Jpn. 16: 227-237.
85. van der Schoot, P., Van Ophemert, J. & Baumgarten, R. (1992). Copulatory stimuli in rats induce heat abbreviation through effects on genitalia but not through effects on central nervous mechanisms supporting the steroid hormone-induced sexual responsiveness. - Behav. Brain Res. 49: 213-223.
86. Viau, V. & Meaney, M.J. (1991). Variations in the hypothalamic-pituitary-adrenal response to stress during the estrous cycle in the rat.- Endocrinology 129: 2503-2511.
87. Walf, A.A., Rhodes, M.E. & Frye, C.A. (2006). Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats.-Neurobiol. Learn. Mem. 86: 35-46.
88. Winland, C., Bolton, J.L., Ford, B., Jampana, S., Tinker, J., Frohardt, R.J., Guarraci, F.A. & Zewail-Foote, M. (2012). "Nice guys finish last": influence of mate choice on reproductive success in Long Evans rats.- Physiol. Behav. 105: 868-876.
89. Xu, X.H., Coats, J.K., Yang, C.F., Wang, A., Ahmed, O.M., Alvarado, M., Izumi, T. & Shah, N.M. (2012). Modular genetic control of sexually dimorphic behaviors.-Cell 148: 596-607.
90. Zewail-Foote, M., Diehl, A., Benson, A., Lee, K.H. & Guarraci, F.A. (2009). Reproductive success and mate choice in Long-Evans rats.- Physiol. Behav. 96: 98-103.