Role of the olfactory systems and importance of learning in the ewes' response to rams or their odors

Reproduction Nutrition Development

Volumn 46, Issue 4, 2006, Pages 401-415

  Gelez, Hélène ^a   Fabre Nys, Claude ^a  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

Author keywords

Experience; LH; Male effect; Olfaction; Ovine

Indexed keywords

LUTEINIZING HORMONE;

ANESTRUS; BEHAVIOR; CONFERENCE PAPER; ENDOCRINE FUNCTION; LEARNING; LUTEINIZING HORMONE RELEASE; NERVE TRACT; NONHUMAN; ODOR; OLFACTORY SYSTEM; OVULATION; SEXUAL BEHAVIOR; SHEEP;

ANIMALS; ESTRUS SYNCHRONIZATION; FEMALE; LEARNING; LUTEINIZING HORMONE; MALE; OLFACTORY PATHWAYS; OVULATION; PERCEPTION; PRACTICE (PSYCHOLOGY); SEASONS; SEX ATTRACTANTS; SEXUAL BEHAVIOR, ANIMAL; SHEEP;

OVIS; OVIS ARIES;

EID: 33748368739     PISSN: 09265287     EISSN: 12979708     Source Type: Journal    
DOI: 10.1051/rnd:2006021     Document Type: Conference Paper

References (99)

1. McClintock MK. Estrous synchrony and its mediation by airborne chemical communication (Rattus norvegicus). Horm Behav 1978, 10: 264-275.
2. Van Der Lee S, Boot LM. Spontaneous pseudopregnancy in mice. Acta Physiol Pharmacol Neerl 1955, 4: 442-444.
3. Whitten WK. Occurrence of anoestrus in mice caged in groups. J Endocrinol 1959, 18: 102-107.
4. Lawton AD, Whitsett JM. Inhibition of sexual maturation by a urinary pheromone in male prairie deer mice. Horm Behav 1979, 13: 128-138.
5. Vandenbergh JG. Effect of the presence of a male on the sexual maturation of female mice. Endocrinology 1967, 81: 345-349.
6. Vandenbergh JG. The influence of the social environment on sexual maturation in male mice. J Reprod Fertil 1971, 24: 383-390.
7. Whitten WK. Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J Endocrinol 1956, 13: 399-404.
8. Bruce HM. A block to pregnancy in the mouse caused by proximity of strange males. J Reprod Fertil 1960, 1: 96-103.
9. Macrides F, Bartke A, Fernandez F, D'Angelo W. Effects of exposure to vaginal odor and receptive females on plasma testosterone in the male hamster. Neuroendocrinology 1974, 15: 355-364.
10. Ryan KD, Schwartz NB. Changes in serum hormone levels associated with male-induced ovulation in group-housed adult female mice. Endocrinology 1980, 106: 959-966.
11. Chemineau P. Effect on oestrus and ovulation of exposing creole goats to the male at three times of the year. J Reprod Fertil 1983, 67: 65-72.
12. Martin GB, Oldham CM, Cognié Y, Pearce DT. The physiological responses of anovulatory ewes to the introduction of rams - A review. Livest Prod Sci 1986, 15: 219-247.
13. Thimonier J, Cognié Y, Lassoued N, Khaldi G. L'effet mâle chez les ovins: une technique actuelle de maîtrise de la reproduction. INRA Prod Anim 2000, 13: 223-231.
14. Brown RE. Odor preference and urine-marking scales in male and female rats: effects of gonadectomy and sexual experience on responses to conspecifics odors. J Comp Physiol Psychol 1977, 91: 1190-1206.
15. Johnston RE, Bronson F. Endocrine control of female mouse odors that elicit luteinizing hormone surges and attraction in males. Biol Reprod 1982, 27: 1174-1180.
16. Petrulis A, Johnston RE. A reevaluation of dimethyl disulfide as a sex attractant in golden hamsters. Physiol Behav 1995, 57: 779-784.
17. Rasmussen LE, Lee TD, Zhang A, Roelofs WL, Daves GD Jr. Purification, identification, concentration and bioactivity of (Z)-7-dodecen-1-yl acetate: sex pheromone of the female Asian elephant, Elephas maximus. Chem Senses 1997, 22: 417-437.
18. Michael RP, Keverne EB. Primate sex pheromones of vaginal origin. Nature 1970, 225: 84-85.
19. Bronson FH. Serum FSH, LH, and prolactin in adult ovariectomized mice bearing silastic implants of estradiol: responses to social cues. Biol Reprod 1976, 15: 147-152.
20. Kamel F, Wright WW, Mock EJ, Frankel AI. The influence of mating and related stimuli on plasma levels of luteinizing hormone, follicle stimulating hormone, prolactin, and testosterone in the male rat. Endocrinology 1977, 101: 421-429.
21. Dluzen DE, Ramirez VD, Carter CS, Getz LL. Male vole urine changes luteinizing hormone-releasing hormone and norepinephrine in female olfactory bulb. Science 1981, 212: 573-575.
22. Knight TW, R LP. Source of ram pheromones that stimulate ovulation in the ewe. Anim Reprod Sci 1980, 3: 133-136.
23. Cohen-Tannoudji, J. Effet du mâle sur la sécrétion gonadotrope (LH) de la brebis (Ovis aries L). Analyse de l'interaction olfactive. Thèse de doctorat, Université de Paris, 1988.
24. Scalia F, Winans SS. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J Comp Neurol 1975, 161: 31-55.
25. Kevetter GA, Winans SS. Connections of the corticomedial amygdala in the golden hamster. II. Efferents of the "olfactory amygdala". J Comp Neurol 1981, 197: 99-111.
26. Kevetter GA, Winans SS. Connections of the corticomedial amygdala in the golden hamster. I. Efferents of the "vomeronasal amygdala". J Comp Neurol 1981, 197: 81-98.
27. Jansen HT, Iwamoto GA, Jackson GL. Central connections of the ovine olfactory bulb formation identified using wheat germ agglutinin-conjugated horseradish peroxidase. Brain Res Bull 1998, 45: 27-39.
28. Brennan PA. The vomeronasal system. Cell Mol Life Sci 2001, 58: 546-555.
29. Keverne EB. Non-olfactory chemoreceptors of the nose: recent advances in understanding the vomeronasal and trigeminal systems. Chem Senses 1986, 11: 119-133.
30. Wysocki CJ, Bean NJ, Beauchamp GK. The vomeronasal system: its role in learning and social behaviour. In: Chemical signals in Vertebrates, Plenum Press, New York, 1986, p 471-485.
31. Martin GB, Oldham CM, Lindsay DR. Increased plasma LH levels in seasonally anovular Merino ewes following the introduction of rams. Anim Reprod Sci 1980, 3: 125-132.
32. Martin GB, Scaramuzzi RJ, Lindsay DR. Effect of the introduction of rams during the anoestrous season on the pulsatile secretion of LH in ovariectomized ewes. J Reprod Fertil 1983, 67: 47-55.
33. Poindron P, Cognie Y, Gayerie F, Orgeur P, Oldham CM, Ravault JP. Changes in gonadotrophins and prolactin levels in isolated (seasonally or lactationally) anovular ewes associated with ovulation caused by the introduction of rams. Physiol Behav 1980, 25: 227-236.
34. Oldham CM, Martin GB, Knight TW. Stimulation of the seasonally anovular Merinos ewes by rams. I. Time from introduction of the rams to the preovulatory surge and ovulation. Anim Reprod Sci 1978, 1: 283-290.
35. Martin GB, Scaramuzzi RJ. The induction of oestrus and ovulation in seasonally anovular ewes by exposure to rams. J Steroid Biochem 1983, 19: 869-875.
36. Oldham CM, Martin GB. Stimulation of the seasonally anovular Merinon ewes by rams. II. Premature regression of ram-induced corpora lutea. Anim Reprod Sci 1978, 1: 291-295.
37. Cohen-Tannoudji J, Einhorn J, Signoret JP. Ram sexual pheromone: first approach of chemical identification. Physiol Behav 1994, 56: 955-961.
38. Karlson P, Luscher M. Pheromones: a new term for a class of biologically active substances. Nature 1959, 183: 55-56.
39. Wilson EO, Bossert WH. Chemical Communication among Animals. Recent Prog Horm Res 1963, 19: 673-716.
40. Gelez H, Fabre-Nys C. The "male effect" in sheep and goats: a review of the respective roles of the two olfactory systems. Horm Behav 2004, 46: 257-271.
41. Maruniak JA, Owen K, Bronson FH, Desjardins C. Urinary marking in female house mice: effects of ovarian steroids, sex experience and type of stimulus. Behav Biol 1975, 13: 211-217.
42. Johnston RE. The causation of two scent-marking behaviour patterns in female hamsters (Mesocricetus auratus). Anim Behav 1977, 25: 317-327.
43. Blissitt MJ, Bland KP, Cottrell DF. Discrimination between the odours of fresh oestrous and non-oestrous ewe urine by rams. Appl Anim Behav Sci 1990, 25: 51-59.
44. Dunbar IF. Olfactory preferences in dogs: the response of male and female beagles to conspecific odors. Behav Biol 1977, 20: 471-481.
45. Signoret JP. Reproductive behaviour of pigs. J Reprod Fertil Suppl 1970, 11: 105.
46. Rasmussen LE, Greenwood DR. Frontalin: a chemical message of musth in Asian elephants (Elephas maximus). Chem Senses 2003, 28: 433-446.
47. Fabre-Nys C, Venier G. Development and use of a method for quantifying female sexual behaviour in ewes. Appl Anim Behav Sci 1987, 17: 289-304.
48. Gelez H, Fabre-Nys C. Neural pathways involved in the endocrine response of anestrous ewes to the male or its odor. Neuroscience 2006 (in press).
49. Gelez H, Archer E, Chesneau D, Magallon T, Fabre-Nys C. Inactivation of the olfactory amygdala prevents the endocrine response to male odour in anoestrus ewes. Eur J Neurosci 2004, 19: 1581-1590.
50. Cohen-Tannoudji J, Lavenet C, Locatelli A, Tillet Y, Signoret JP. Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour. J Reprod Fertil 1989, 86: 135-144.
51. Keverne EB. Pheromonal influences on the endocrine regulation of reproduction. Trends Neurosci 1983, 6: 381-384.
52. Halem HA, Cherry JA, Baum MJ. Vomeronasal neuroepithelium and forebrain Fos responses to male pheromones in male and female mice. J Neurobiol 1999, 39: 249-263.
53. Kelliher KR, Liu YC, Baum MJ, Sachs BD. Neuronal Fos activation in olfactory bulb and forebrain of male rats having erections in the presence of inaccessible estrous females. Neuroscience 1999, 92: 1025-1033.
54. Beltramino C, Taleisnik S. Release of LH in the female rat by olfactory stimuli. Effect of the removal of the vomeronasal organs or lesioning of the accessory olfactory bulbs. Neuroendocrinology 1983, 36: 53-58.
55. Coquelin A, Clancy AN, Macrides F, Noble EP, Gorski RA. Pheromonally induced release of luteinizing hormone in male mice: involvement of the vomeronasal system. J Neurosci 1984, 4: 2230-2236.
56. Wysocki CJ, Katz Y, Bernhard R. Male vomeronasal organ mediates female-induced testosterone surges in mice. Biol Reprod 1983, 28: 917-922.
57. Hudson R, Distel H. Pheromonal release of suckling in rabbits does not depend on the vomeronasal organ. Physiol Behav 1986, 37: 123-128.
58. Domes KM, Adkins-Regan E, Halpern BP. Sensitivity and behavioral responses to the pheromone androsterone are not mediated by the vomeronasal organ in domestic pigs. Brain Behav Evol 1997, 49: 53-62.
59. Kelliher KR, Baum MJ. Nares occlusion eliminates heterosexual partner selection without disrupting coitus in ferrets of both sexes. J Neurosci 2001, 21: 5832-5840.
60. Fiber JM, Adames P, Swann JM. Pheromones induce c-fos in limbic areas regulating male hamster mating behavior. Neuroreport 1993, 4: 871-874.
61. Fewell GD, Meredith M. Experience facilitates vomeronasal and olfactory influence on Fos expression in medial preoptic area during pheromone exposure or mating in male hamsters. Brain Res 2002, 941: 91-106.
62. Beauchamp GK, Doty RL, Moulton DG, Mugford RA. The pheromone concept in mammalian chemical communication: a critique. Doty RL (Ed), Academic Press, New York, 1976.
63. Carr WJ, Loeb LS, Dissinger ML. Responses of rats to sex odors. J Comp Physiol Psychol 1965, 59: 370-377.
64. Doty RL, Dunbar I. Attraction of beagles to conspecific urine, vaginal and anal sac secretion odors. Physiol Behav 1974, 12: 825-833.
65. Hayashi S, Kimura T. Sex-attractant emitted by female mice. Physiol Behav 1974, 13: 563-567.
66. Dizinno G, Whitney G, Nyby J. Ultrasonic vocalizations by male mice (Mus musculus) to female sex pheromone: experiential determinants. Behav Biol 1978, 22: 104-113.
67. Sachs BD. Erection evoked in male rats by airborne scent from estrous females. Physiol Behav 1997, 62: 921-924.
68. Colby DR, Vandenberg JG. Regulatory effects of urinary pheromones on puberty in the mouse. Biol Reprod 1974, 11: 268-279.
69. Carter CS, Getz LL, Gavish L, McDermott JL, Arnold P. Male-related pheromones and the activation of female reproduction in the prairie vole (Microtus ochrogaster). Biol Reprod 1980, 23: 1038-1045.
70. Reasner DS, Johnston RE. Acceleration of reproductive development in female Djungarian hamsters by adult males. Physiol Behav 1988, 43: 57-64.
71. Izard MK, Vandenbergh JG. The effects of bull urine on puberty and calving date in crossbred beef heifers. J Anim Sci 1982, 55: 1160-1168.
72. Pfeiffer CA, Johnston RE. Hormonal and behavioral responses of male hamsters to females and female odors: roles of olfaction, the vomeronasal system, and sexual experience. Physiol Behav 1994, 55: 129-138.
73. Macrides F, Bartke A, Dalterio S. Strange females increase plasma testosterone levels in male mice. Science 1975, 189: 1104-1106.
74. Maruniak JA, Bronson FH. Gonadotropic responses of male mice to female urine. Endocrinology 1976, 99: 963-969.
75. Keverne EB. The vomeronasal organ. Science 1999, 286: 716-720.
76. Wysocki CJ, Lepri JJ. Consequences of removing the vomeronasal organ. J Steroid Biochem Mol Biol 1991, 39: 661-669.
77. Meredith M. Vomeronasal organ removal before sexual experience impairs male hamster mating behavior. Physiol Behav 1986, 36: 737-743.
78. Bean NJ. Olfactory and vomeronasal mediation of ultrasonic vocalizations in male mice. Physiol Behav 1982, 28: 31-37.
79. Datiche F, Roullet F, Cattarelli M. Expression of Fos in the piriform cortex after acquisition of olfactory learning: an immunohistochemical study in the rat. Brain Res Bull 2001, 55: 95-99.
80. Hess US, Gall CM, Granger R, Lynch G. Differential patterns of c-fos mRNA expression in amygdala during successive stages of odor discrimination learning. Learn Mem 1997, 4: 262-283.
81. Tronel S, Sara SJ. Mapping of olfactory memory circuits: region-specific c-fos activation after odor-reward associative learning or after its retrieval. Learn Mem 2002, 9: 105-111.
82. Gelez H, Archer E, Chesneau D, Lindsay D, Fabre-Nys C. Role of experience in the neuroendocrine control of ewes' sexual behavior. Horm Behav 2004, 45: 190-200.
83. Gelez H, Archer E, Chesneau D, Campan R, Fabre-Nys C. Importance of learning in the response of ewes to male odor. Chem Senses 2004, 29: 555-563.
84. Vandenbergh JG. Male odor accelerates female sexual maturation in mice. Endocrinology 1969, 84: 658-660.
85. Johnston RE. Sexual attraction function of golden hamster vaginal secretion. Behav Biol 1974, 12: 111-117.
86. Jemiolo B, Xie TM, Novotny M. Sociosexual olfactory preference in female mice: attractiveness of synthetic chemosignals. Physiol Behav 1991, 50: 1119-1122.
87. Moncho-Bogani J, Lanuza E, Hernandez A, Novejarque A, Martinez-Garcia F. Attractive properties of sexual pheromones in mice: innate or learned? Physiol Behav 2002, 77: 167-176.
88. Banks EM. Some aspects of sexual behavior in domestic sheep, Bovis aries. Behav 1964, 23: 249-279.
89. Ladewig J, Price EO, Hart BL. Flehmen in male goats: role in sexual behavior. Behav Neural Biol 1980, 30: 312-322.
90. Bland KP, Jubilan BM. Correlation of flehmen by male sheep with female behaviour and oestrus. Anim Behav 1987, 35: 735-738.
91. Stevens K, Perry GC, Long SE. Effect of ewe urine and vaginal secretions on ram investigative behaviour. J Chem Ecol 1982, 8: 23-28.
92. Johnston RE. Olfactory preferences, scent marking, and "proceptivity" in female hamsters. Horm Behav 1979, 13: 21-39.
93. Cohen-Tannoudji J, Locatelli A, Signoret JP. Non-pheromonal stimulation by the male of LH release in the anoestrous ewe. Physiol Behav 1986, 36: 921-924.
94. Signoret JP, Fulkerson WJ, Lindsay DR. Effectiveness of testosterone treated wethers and ewes as teasers. Appl Anim Ethol 1982, 9: 37-45.
95. Nyby J, Whitney G, Schmitz S, Dizinno G. Postpubertal experience establishes signal value of mammaliam sex odor. Behav Biol 1978, 22: 545-552.
96. Kippin TE, Pfaus JG. The development of olfactory conditioned ejaculatory preferences in the male rat. I. Nature of the unconditioned stimulus. Physiol Behav 2001, 73: 457-469.
97. Kippin TE, Pfaus JG. The nature of the conditioned response mediating olfactory conditioned ejaculatory preference in the male rat. Behav Brain Res 2001, 122: 11-24.
98. Graham JM, Desjardins C. Classical conditioning: induction of luteinizing hormone and testosterone secretion in anticipation of sexual activity. Science 1980, 210: 1039-1041.
99. Kelliher KR, Chang YM, Wersinger SR, Baum MJ. Sex difference and testosterone modulation of pheromone-induced Neuronal Fos in the Ferret's main olfactory bulb and hypothalamus. Biol Reprod 1998, 5: 1454-1463.