The "male effect" in sheep and goats: A review of the respective roles of the two olfactory systems

Hormones and Behavior

Volumn 46, Issue 3, 2004, Pages 257-271

  Gelez, H ^a   Fabre Nys, C ^a  

^a CNRS   (France)

Author keywords

Amygdala; Experience; LH; Main olfactory system; Male effect; Sheep; Vomeronasal organ

Indexed keywords

LUTEINIZING HORMONE; PHEROMONE;

AMYGDALOID NUCLEUS; ANESTRUS; GOAT; HORMONE RELEASE; LEARNING; NONHUMAN; OLFACTORY BULB; OLFACTORY SYSTEM; OVULATION; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SEXUAL BEHAVIOR; SHEEP; SMELLING; VOMERONASAL ORGAN;

EID: 8444241079     PISSN: 0018506X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2004.05.002     Document Type: Article

References (141)

1. Barfield R.J. Gonadotrophic hormone secretion in the female ring dove in response to visual and auditory stimulation by the male. J. Endocrinol. 28:1971;320-328
2. Bean N.J. Olfactory and vomeronasal mediation of ultrasonic vocalizations in male mice. Physiol. Behav. 28:1982;31-37
3. Beauchamp G.K., Doty R.L., Moulton D.G., Mugford R.A. The pheromone concept in mammalian chemical communication: a critique. Doty R.L. Mammalian Olfaction, Reproductive Processes and Behavior. 1976;Academic Press, New York
4. Bellringer J.F., Pratt P.M., Keverne E.B. Involvement of the vomeronasal organ and prolactin in pheromonal induction of delayed implantation in mice. J. Reprod. Fertil. 59:1980;223-228
5. Belluscio L., Koentges G., Axel R., Dulac C. A map of pheromone activation in the mammalian brain. Cell. 97:1999;209-220
6. 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. 36:1983;53-58
7. Bentley G.E., Wingfield J.C., Morton M.L., Ball G.F. Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song. Horm. Behav. 37:2000;179-189
8. Blissitt M.J., Bland K.P., Cottrell D.F. Discrimination between the odours of fresh oestrous and non-oestrous ewe urine by rams. Appl. Anim. Behav. Sci. 25:1990;51-59
9. Booth K.K., Katz L.S. Role of the vomeronasal organ in neonatal offspring recognition in sheep. Biol. Reprod. 63:2000;953-958
10. Brennan P.A. The vomeronasal system. Cell. Mol. Life Sci. 58:2001;546-555
11. Bronson F.H., Serum F.S.H. LH and prolactin in adult ovariectomized mice bearing silastic implant of estradiol: responses to social cues. Biol. Reprod. 15:1976;147-152
12. Brown R.E. 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. 91:1977;1190-1206
13. Brownlee R.G., Silverstein R.M., Muller-Schwarze D., Singer A.G. Isolation, identification and function of the chief component of the male tarsal scent in black-tailed deer. Nature. 221:1969;284-285
14. Bruce H.M. A block to pregnancy in the mouse caused by proximity of strange males. J. Reprod. Fertil. 1:1960;96-103
15. Carter C.S., Getz L.L., Gavish L., McDermott J.L., Arnold P. Male-related pheromones and the activation of female reproduction in the prairie vole (Microtus ochrogaster). Biol. Reprod. 23:1980;1038-1045
16. Chaillou E., Baumont R., Tramu G., Tillet Y. Effect of feeding on Fos protein expression in sheep hypothalamus with special reference to the supraoptic and paraventricular nuclei: an immunohistochemical study. Eur. J. Neurosci. 12:2000;4515-4524
17. Chemineau P. Effect on oestrus and ovulation of exposing Creole goats to the male at three times of the year. J. Reprod. Fertil. 67:1983;65-72
18. Chemineau P., Lévy F., Thimonier J. Effects of anosmia on LH secretion, ovulation and oestrous behaviour induced by males in the anovular Creole goat. Anim. Reprod. Sci. 10:1986;125-132
19. Clancy A.N., Coquelin A., Macrides F., Gorski R.A., Noble E.P. Sexual behavior and aggression in male mice: involvement of the vomeronasal system. J. Neurosci. 4:1984;2222-2229
20. Claus R., Over R., Dehnard M. Effect of male odour on LH secretion and the induction of ovulation in seasonally anoestrous goats. Anim. Reprod. Sci. 22:1990;27-38
21. Cohen-Tanoudji J., Locatelli A., Signoret J.P. Non-pheromonal stimulation by the male of LH release in the anoestrous ewe. Physiol. Behav. 36:1986;921-924
22. Cohen-Tanoudji J., Lavenet C., Locatelli A., Tillet Y., Signoret J.P. Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour. J. Reprod. Fertil. 86:1989;135-144
23. Cohen-Tanoudji J., Einhorn J., Signoret J.P. Ram sexual pheromone: first approach of chemical identification. Physiol. Behav. 56:1994;955-961
24. Colby D.R., Vandenbergh J.G. Regulatory effects of urinary pheromones on puberty in the mouse. Biol. Reprod. 11:1974;268-279
25. Coquelin A., Clancy A.N., Macrides F., Noble E.P., Gorski R.A. Pheromonally induced release of luteinizing hormone in male mice: involvement of the vomeronasal system. J. Neurosci. 4:1984;2230-2236
26. Cummings D.M., Emge D.K., Small S.L., Margolis F.L. Pattern of olfactory bulb innervation returns after recovery from reversible peripheral deafferentation. J. Comp. Neurol. 421:2000;362-373
27. Curtis R.F., Ballantine J.A., Keverne E.B., Bonsall R.W., Michael R.P. Identification of primate sexual pheromones and the properties of synthetic attractants. Nature. 232:1971;396-398
28. 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. 55:2001;95-99
29. Dizinno G., Whitney G., Nyby J. Ultrasonic vocalizations by male mice (Mus musculus) to female sex pheromone: experiential determinants. Behav. Biol. 22:1978;104-113
30. Dluzen D.E., Ramirez V.D., Carter C.S., Getz L.L. Male vole urine changes luteinizing hormone-releasing hormone and norepinephrine in female olfactory bulb. Science. 212:1981;573-575
31. Dorries K.M., Adkins-Regan E., Halpern B.P. Sensitivity and behavioral responses to the pheromone, androstenone, are not mediated by the vomeronasal organ in domestic pigs. Brain Behav. Evol. 49:1997;53-62
32. Dudley C.A., Moss R.L. Activation of an anatomically distinct subpopulation of accessory olfactory bulb neurons by chemosensory stimulation. Neuroscience. 91:1999;1549-1556
33. Dulac C., Axel R. A novel family of genes encoding putative pheromone receptors in mammals. Cell. 83:1995;195-206
34. Dunbar I.F. Olfactory preferences in dogs: the response of male and female beagles to conspecifics odors. Behav. Biol. 26:1977;471-481
35. Fabre-Nys C., Venier G. Development and use of a method for quantifying female sexual behaviour in ewes. Appl. Anim. Behav. Sci. 17:1987;289-304
36. Fewell G.D., 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. 941:2002;91-106
37. Fiber J.M., Adames P., Swann J.M. Pheromones induce c-fos in limbic areas regulating male hamster mating behavior. NeuroReport. 4:1993;871-874
38. Fletcher I.C., Lindsay D.R. Sensory involvement in the mating behaviour of domestic sheep. Anim. Behav. 16:1968;410-414
39. Gelez H., Chesneau D., Fabre-Nys C. Which structures are activated in the anestrous female brain by the male or its odour? 3rd Forum of European Neuroscience, Paris:2002
40. Gelez H., Archer E., Chesneau D., Magallon T., Fabre-Nys C. Inactivation of the olfactory amygdala prevents endocrine response to male odour in anestrus ewes. Eur. J. Neurosci. 19:2004;1581-1590
41. Gelez H., Archer E., Chesneau D., Lindsay D., Fabre-Nys C. Role of experience in the neuroendocrine control of ewes' sexual behavior. Horm. Behav. 45:2004;190-200
42. 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;. (in press)
43. Halem H.A., Cherry J.A., Baum M.J. Vomeronasal neuroepithelium and forebrain fos responses to male pheromones in male and female mice. J. Neurobiol. 39:1999;249-263
44. Harding J.W., Getchell T.V., Margolis F.L. Denervation of the primary olfactory pathway in mice, V. Long-term effect of intranasal ZnSO4 irrigation on behavior, biochemistry and morphology. Brain Res. 140:1978;271-285
45. Hayashi S., Kimura T. Sex-attractant emitted by female mice. Physiol. Behav. 13:1974;563-567
46. Hess U.S., Gall C.M., Granger R., Lynch G. Differential patterns of c-fos mRNA expression in amygdala during successive stages of odor discrimination learning. Learn. Mem. 4:1997;262-283
47. Hudson R., Distel H. Pheromonal release of suckling in rabbit does not depend on the vomeronasal organ. Physiol. Behav. 37:1986;123-128
48. Inamura K., Kashiwayanagi M., Kurihara K. Regionalization of Fos immunostaining in rat accessory olfactory bulb when the vomeronasal organ was exposed to urine. Eur. J. Neurosci. 11:1999;2254-2260
49. Iwata E., Kikusui T., Takeuchi Y., Mori Y. Substances derived from 4-ethyl octanoic acid account for primer pheromone activity for the "male effect" in goats. J. Vet. Med. Sci. 65:2003;1019-1021
50. Jansen H.T., Iwamoto G.A., Jackson G.L. Central connections of the ovine olfactory bulb formation identified using wheat germ agglutinin-conjugated horseradish peroxidase. Brain Res. Bull. 45:1998;27-39
51. Jia C., Halpern M. Subclasses of vomeronasal receptor neurons: differential expression of G proteins (Gi alpha 2 and G(o alpha)) and segregated projections to the accessory olfactory bulb. Brain Res. 719:1996;117-128
52. Johns M.A., Feder H.H., Komisaruk B.R., Mayer A.D. Urine-induced reflex ovulation in anovulatory rats may be a vomeronasal effect. Nature. 272:1978;446-448
53. Johnston R.E. The causation of two scent-marking behaviour patterns in female hamsters (Mesocricetus auratus). Anim. Behav. 25:1977;317-327
54. Johnston R.E. Pheromones, the vomeronasal system, and communication. From hormonal responses to individual recognition. Ann. N. Y. Acad. Sci. 855:1998;333-348
55. Johnston R.E., Bronson F. Endocrine control of female mouse odors that elicit luteinizing hormone surges and attraction in male. Biol. Reprod. 27:1982;1174-1180
56. Kaba H., Rosser A., Keverne B. Neural basis of olfactory memory in the context of pregnancy block. Neuroscience. 32:1989;657-662
57. Kamel F., Wright W.W., Mock E.J., Frankel A.I. The influence of mating and related stimuli on plasma of luteinizing hormone, follicle stimulating hormone, prolactin, and testosterone in the male rat. Endocrinology. 101:1977;421-429
58. Karlson P., Lüscher M. "Pheromones": a new term for a class of biologically active substances. Nature. 183:1959;55-56
59. Kelliher K.R., Baum M.J. Nares occlusion eliminates heterosexual partner selection without disrupting coitus in ferrets of both sexes. J. Neurosci. 21:2001;5832-5840
60. Kelliher K.R., Chang Y.M., Wersinger S.R., Baum M.J. Sex difference and testosterone modulation of pheromone-induced neuronal Fos in the Ferret's main olfactory bulb and hypothalamus. Biol. Reprod. 59:1998;1454-1463
61. Kelliher K.R., Liu Y.C., Baum M.J., Sachs B.D. Neuronal Fos activation in olfactory bulb and forebrain of male rats having erections in the presence of inaccessible estrous females. Neuroscience. 92:1999;1025-1033
62. Keverne E.B. Pheromonal influences on the endocrine regulation of reproduction. Trends Neurosci. 6:1983;381-384
63. Keverne E.B. Non-olfactory chemoreceptors of the nose: recent advances in understanding the vomeronasal and trigeminal systems. Chem. Senses. 11:1986;119-133
64. Kevetter G.A., Winans S.S. Connections of the corticomedial amygdala in the golden hamster: I. Efferents of the "vomeronasal amygdala" J. Comp. Neurol. 197:1981;81-98
65. Kevetter G.A., Winans S.S. Connections of the corticomedial amygdala in the golden hamster: II. Efferents of the "olfactory amygdala" J. Comp. Neurol. 197:1981;99-111
66. Kirn J., Floody O.R. Differential effects of lesions in three limbic areas on ultrasound production and lordosis by female hamsters. Behav. Neurosci. 99:1985;1142-1152
67. Knight T.W., Lynch P.R. Source of ram pheromones that stimulate ovulation in the ewe. Anim. Reprod. Sci. 3:1980;133-136
68. Kumar A., Dudley C.A., Moss R.L. Functional dichotomy within the vomeronasal system: distinct zones of neuronal activity in the accessory olfactory bulb correlate with sex-specific behaviors. J. Neurosci. 19:1999;1-6
69. Ladewig J., Price E.O., Hart B. Flehmen in male goats: role in sexual behavior. Behav. Neural Biol. 30:1980;312-322
70. Lawton A.D., Whitsett J.M. Inhibition of sexual maturation by a urinary pheromone in male prairie deer mice. Horm. Behav. 13:1979;128-138
71. Lévy F., Locatelli A., Piketty V., Tillet Y., Poindron P. Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes. Physiol. Behav. 57:1995;97-104
72. Lindsay D.R. Mating behaviour of ewes and its effect on mating efficiency. Anim. Behav. 14:1966;419-424
73. Lloyd-Thomas A., Keverne E.B. Role of the brain and accessory olfactory system in the block to pregnancy in mice. Neuroscience. 7:1982;907-913
74. Lomas D.E., Keverne E.B. Role of the vomeronasal organ and prolactin in the acceleration of puberty in female mice. J. Reprod. Fertil. 66:1982;101-107
75. Ma W., Miao Z., Novotny M.V. Induction of estrus in grouped female mice (Mus domesticus) by synthetic analogues of preputial gland constituents. Chem. Senses. 24:1999;289-293
76. Mackay-Sim A., Rose J.D. Removal of the vomeronasal organ impairs lordosis in female hamsters: effect is reversed by LHRH. Neuroendocrinology. 42:1986;489-493
77. 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. 15:1974;355-364
78. Macrides F., Clancy A.N., Singer A.G., Agosta W.C. Male hamster investigatory and copulatory responses to vaginal discharge: an attempt to impart sexual significance to an arbitrary chemosensory stimulus. Physiol. Behav. 33:1984;627-632
79. Martin G.B., Scaramuzzi R.J. The induction of oestrus and ovulation in seasonally anovular ewes by exposure to rams. J. Steroid Biochem. 19:1983;869-875
80. Martin G.B., Scaramuzzi R.J., Lindsay D.R. Increased plasma LH levels in seasonally anovular merino ewes following the introduction of rams. Anim. Reprod. Sci. 3:1980;125-132
81. Martin G.B., Scaramuzzi R.J., Lindsay D.R. Effect of the introduction of rams during the anoestrous season on the pulsatile secretion of LH in ovariectomized ewes. J. Reprod. Fertil. 67:1983;47-55
82. Martin G.B., Oldham C.M., Cognié Y., Pearce D.T. The physiological responses of anovulatory ewes to the introduction of rams - A review. Livest. Prod. Sci. 15:1986;219-247
83. Maruniak J.A., Owen K., Bronson F.H., Desjardins C. Urinary marking in female house mice: effects of ovarian steroids, sex experience, and type of stimulus. Behav. Biol. 13:1975;211-217
84. Masco D.H., Carrer H.F. Sexual receptivity in female rats after lesion or stimulation in different amygdaloid nuclei. Physiol. Behav. 24:1980;1073-1080
85. Matsunami H., Buck L.B. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell. 90:1997;775-784
86. McClintock M.K. Estrous synchrony and its mediation by airborne chemical communication (Rattus norvegicus). Horm. Behav. 10:1978;264-276
87. Melrose D.R., Reed H.C.B., Patterson R.L.S. Androgen steroids associated with boar odour as an aid to the detection of oestrus in pig artificial insemination. Br. Vet. J. 127:1971;497-502
88. Meredith M. Vomeronasal organ removal before sexual experience impairs male hamster mating behavior. Physiol. Behav. 36:1986;737-743
89. Meredith M. Vomeronasal, olfactory, hormonal convergence in the brain. Cooperation or coincidence? Ann. N. Y. Acad. Sci. 855:1998;349-361
90. Meredith M., Marques D.M., O'Connell R.J., Stern F.L. Vomeronasal pump: significance for male hamster sexual behavior. Science. 207:1980;1224-1226
91. Michael R.P., Keverne E.B. Primate sex pheromones of vaginal origin. J. Endocrinol. 46:1970;xx-xxi
92. Morgan P.D., Arnold G.W., Lindsay D.R. A note on the mating behaviour of ewes with various senses impaired. J. Reprod. Fertil. 30:1972;151-152
93. Mori K., von Campenhausen H., Yoshihara Y. Zonal organization of the mammalian main and accessory olfactory systems. Philos. Trans. R. Soc. Lond., B Biol. Sci. 355:2000;1801-1812
94. Muller-Schwarze D. Pheromones in black-tailed deer. Anim. Behav. 19:1971;141-152
95. Novotny M.V., Ma W., Wiesler D., Zidek L. Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein. Proc. R. Soc. Lond., B Biol. Sci. 266:1999;2017-2022
96. Nyby J., Wysocki C.J., Whitney G., Dizinno G. Pheromonal regulation of male mouse ultrasonic courtship (Mus musculus). Anim. Behav. 25:1977;333-341
97. Oldham C.M., Martin G.B. Stimulation of the seasonally anovular merino ewes by rams: II. Premature regression of ram-induced corpora lutea. Anim. Reprod. Sci. 1:1978;291-295
98. Oldham C.M., Martin G.B., Knight T.W. 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. 1:1978;283-290
99. Over R., Cohen-Tannoudji J., Dehnhard M., Claus R., Signoret J.P. Effect of pheromones from male goats on LH-secretion in anoestrous ewes. Physiol. Behav. 48:1990;665-668
100. Perkins A., Fitzgerald J.A. The behavioral component of the ram effect: the influence of ram sexual behavior on the induction of œstrus in anovulatory ewes. J. Anim. Sci. 72:1994;51-55
101. Petrulis A., Johnston R.E. A reevaluation of dimethyl disulfide as a sex attractant in golden hamsters. Physiol. Behav. 57:1995;779-784
102. Petrulis A., Johnston R.E. Lesions centered on the medial amygdala impair scent-marking and sex-odor recognition but spare discrimination of individual odors in female golden hamsters. Behav. Neurosci. 113:1999;345-357
103. Pfeiffer C.A., Johnston R.E. Hormonal and behavioral responses of male hamsters to females and female odors: roles of olfaction, the vomeronasal system, and sexual experience. Physiol. Behav. 55:1994;129-138
104. Poindron P. Méthode de suppression réversible de l'odorat chez la brebis and vérification de l'anosmie au moyen d'une épreuve comportementale. Ann. Biol. Anim., Biochim., Biophys. 14:1974;411-415
105. Poindron P., Cognié Y., Gayerie F., Orgeur P., Oldham C.M., Ravault J.P. Changes in gonadotrophins and prolactin levels in isolated (seasonally or lactationally) anovular ewes associated with ovulation caused by the introduction of rams. Physiol. Behav. 25:1980;227-236
106. Rasmussen L.E., Greenwood D.R. Frontalin: a chemical message of musth in Asian elephants (Elephas maximus). Chem. Senses. 28:2003;433-446
107. Rasmussen L.E., Lee T.D., Zhang A., Roelofs W.L., Daves G.D. Jr. Purification, identification, concentration and bioactivity of (Z)-7-dodecen-1-yl acetate: sex pheromone of the female Asian elephant, Elephas maximus. Chem. Senses. 22:1997;417-437
108. Rodriguez I., Feinstein P., Monbaerts P. Variable patterns of axonal projections of sensory neurons in the mouse vomeronasal organ. Cell. 97:1999;199-208
109. Rodriguez Iglesias R.M., Ciccioli N.H., Irazoqui H., Rodriguez B.T. Importance of behavioural stimuli in ram-induced ovulation in seasonally anovular corriedale ewes. Appl. Anim. Behav. Sci. 30:1991;323-332
110. Rollmann S.M., Houck L.D., Feldhoff R.C. Proteinaceous pheromone affecting female receptivity in a terrestrial salamander. Science. 285:1999;1907-1909
111. Romero P.A., Beltramino C.A., Carrer H.F. Participation of the olfactory system in the control of approach behavior of the female rat to the male. Physiol. Behav. 47:1990;685-690
112. Ryan K.D., Schwartz N.B. Changes in serum hormones levels associated with male-induced ovulation in group-housed female mice. Endocrinology. 105:1980;959-966
113. Sachs B.D. Erection evoked in male rats by airborne scent from estrous females. Physiol. Behav. 62:1997;921-924
114. Scalia F., Winans S.S. The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. J. Comp. Neurol. 161:1975;31-56
115. Schaal B., Coureaud G., Langlois D., Ginies C., Semon E., Perrier G. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature. 424:2003;68-72
116. Schwob J.E., Youngentob S.L., Mezza R.C. Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J. Comp. Neurol. 359:1995;15-37
117. Signoret J.P. Reproductive behaviour of pigs. J. Reprod. Fertil., Suppl. 11:1970;105-117
118. Signoret J.P. Rôle des différentes informations sensorielles dans l'attraction de la femelle en œstrus par le mâle chez les porcins. Ann. Biol. Anim., Biochim., Biophys. 14:1974;747-755
119. Signoret J.P. The influence of the ram effect on the breeding activity of ewes and its underlying physiology. Oldham C.M., Martin G.B., Purvis I.W. Reproductive Physiology of Merino Sheep. Concepts and Consequences. 1990;School of Agriculture (Animal Science), Perth, Australia
120. Signoret J.P., Fulkerson W.J., Lindsay D.R. Effectiveness of testosterone treated wethers and ewes as teasers. Appl. Anim. Ethol. 9:1982;37-45
121. Singer A.G. A chemistry of mammalian pheromones. J. Steroid Biochem. Mol. Biol. 39:1991;627-632
122. Singer A.G., Agosta W.C., O'Connell R.J., Pfaffmann C., Bowen D.V., Field F.H. Dimethyl disulfide: an attractant pheromone in hamster vaginal secretion. Science. 191:1976;948-950
123. Sugiyama T., Sasada H., Masaki J., Yamashita K. Unusual fatty acids with specific odor from mature male goat. Agric. Biol. Chem. 45:1981;2655-2658
124. Takigami S., Mori Y., Ichikawa M. Projection pattern of vomeronasal neurons to the accessory olfactory bulb in goats. Chem. Senses. 25:2000;387-393
125. 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. 13:2000;223-231
126. Trinh K., Storm D.R. Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nat. Neurosci. 6:2003;519-525
127. Tronel S., Sara S.J. Mapping of olfactory memory circuits: region-specific c-fos activation after odor-reward associative learning or after its retrieval. Learn. Mem. 9:2002;105-111
128. Vandenbergh J.G. Effect of the presence of a male on the sexual maturation of female mice. Endocrinology. 81:1967;345-349
129. Vandenbergh J.G. The influence of the social environment on sexual maturation in male mice. J. Reprod. Fertil. 24:1971;383-390
130. Van Der Lee S., Boot L.M. Spontaneous pseudopregnancy in mice. Acta Physiol. Pharmacol. Neerl. 4:1955;442-444
131. Wakabayashi Y., Mori Y., Ichikawa M., Yazaki K., Hagino-Yamagishi K. A putative pheromone receptor gene is expressed in two distinct olfactory organs in goats. Chem. Senses. 27:2002;207-213
132. Walkden-Brown S.W., Restall H., Henniawati The male effect in the Australian cashmere goat: 1. Ovarian and behavioural response of seasonally anovulatory does following the introduction of bucks. Anim. Reprod. Sci. 32:1993;41-53
133. Walkden-Brown S.W., Restall H., Henniawati The male effect in the Australian cashmere goat: 2. Role of olfactory cues from the male. Anim. Reprod. Sci. 32:1993;55-67
134. Wersinger S.R., Baum M.J. Sexually dimorphic processing of somatosensory and chemosensory inputs to forebrain LHRH neurons in mated ferrets. Endocrinology. 138:1997;1121-1129
135. Whitten W.K. Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J. Endocrinol. 13:1956;399-404
136. Whitten W.K. Occurrence of anestrus in mice caged in groups. J. Endocrinol. 18:1959;102-107
137. Widowski T.M., Lo Fo Wong D.M., Duncan I.J. Rearing with males accelerates onset of sexual maturity in female domestic fowl. Poult. Sci. 77:1998;150-155
138. Wilson E.O., Bossert W.H. Chemical communication among animals. Recent Prog. Horm. Res. 19:1963;673-710
139. Wysocki C.J., Lepri J.J. Consequences of removing the vomeronasal organ. J. Steroid Biochem. Mol. Biol. 39:1991;661-669
140. Wysocki C.J., Katz Y., Bernhard R. Male vomeronasal organ mediates female-induced testosterone surges in mice. Biol. Reprod. 28:1983;917-922
141. Wysocki C.J., Bean N.J., Beauchamp G.K. The vomeronasal system: its role in learning and social behaviour. Duvall D., Muller-Schwarze D., Silverstein R.M. Chemical Signals in Vertebrates. 1986;471-485 Plenum, New York