Male hamster copulatory responses to a high molecular weight fraction of vaginal discharge: Effects of vomeronasal organ removal
Abstract
The importance of the vomeronasal (accessory olfactory) system for the copulatory responses of male hamsters to a high molecular weight fraction (HMF) of vaginal discharge was assessed in animals that had their vomeronasal organs (VNO) removed. These organs were extirpated bilaterally using an oral approach through the palate so as to eliminate the peripheral afferents to the accessory olfactory bulb (AOB) with minimal or no damage to the main olfactory system. The selective peripheral deafferentation procedure was verified by applying horseradish peroxidase intranasally following intraperitoneal injections of epinephrine to facilitate the vomeronasal pumping mechanism that draws fluids into the VNO. Heavy, bilateral anterograde labeling was evident in the olfactory nerve afferents within the main olfactory bulb of males that had their VNO removed and of animals that received sham surgery. Sham-operated males also had heavy, bilateral labeling in the vomeronasal nerve afferents within the AOB, whereas no such labeling occurred among animals with bilateral removal of the VNO. In sham-operated animals, both the HMF and the unfractionated discharge significantly increased the incidence of intromission attempts toward anesthetized males (surrogate females) whose hindquarters were scented with these stimuli. The unfractionated discharge also produced a significant elevation of overt copulatory behavior in males with selective peripheral deafferentation of the vomeronasal system, w…
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Among species where some chemical communication can be assigned to the vomeronasal sensory pathway, there are a number of examples where the signals appear to be nonvolatile and to be transmitted by direct contact between receiver and stimulus source.
“Among species where some chemical communication can be assigned to the vomeronasal sensory pathway there are a number of examples where the signals appear to be nonvolatile and to be transmitted by direct contact between receiver and stimulus source (Meredith, 1983;Clancy et al., 1984).”
From Human Vomeronasal Organ Function: A Critical Review of Best and Worst Cases (2001) · cites this paper as Clancy et al., 1984
Cites
Role of the brain and accessory olfactory system in the block to pregnancy in mice
Lloyd-Thomas, A., & Keverne, E. B. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90051-3 · Cited by 138 · see citing works
Coquelin, A., Clancy, A., Macrides, F., Noble, E., & Gorski, R. (1984) · The Journal of Neuroscience · doi:10.1523/jneurosci.04-09-02230.1984 · Cited by 127 · see citing works
Self-citationSensory Physiology of Pheromone Communication
Meredith, M. (1983) · Pheromones and Reproduction in Mammals · doi:10.1016/b978-0-12-710780-6.50014-5 · Cited by 113 · see citing works
Luteinizing hormone‐releasing hormone (LHRH) in rat olfactory systems
Witkin, J. W., & Silverman, A. (1983) · Journal of Comparative Neurology · doi:10.1002/cne.902180407 · Cited by 96 · see citing works
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Tirindelli, R., Dibattista, M., Pifferi, S., & Menini, A. (2009) · Physiological Reviews · doi:10.1152/physrev.00037.2008 · Cited by 370 · see citing works
Human Vomeronasal Organ Function: A Critical Review of Best and Worst Cases
Meredith, M. (2001) · Chemical Senses · doi:10.1093/chemse/26.4.433 · Cited by 280 · see citing works
“Among species where some chemical communication can be assigned to the vomeronasal sensory pathway there are a number of examples where the signals appear to be nonvolatile and to be transmitted by direct contact between receiver and stimulus source (Meredith, 1983; Clancy et al., 1984).”
BackgroundVomeronasal organ removal before sexual experience impairs male hamster mating behavior.
Meredith, M. (1986) · Physiology and Behavior · doi:10.1016/0031-9384(86)90362-8 · Cited by 186 · see citing works
Fernandez-Fewell, G. D., & Meredith, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03643.1994 · Cited by 176 · see citing works
“(Clancy et al., 1984).”
Serby, M., & Chobor, K. L. (1992) · Springer: New York · doi:10.1007/978-1-4612-2836-3 · Cited by 169 · see citing works
Is the vomeronasal system really specialized for detecting pheromones?
Baxi, K. N., Dorries, K. M., & Eisthen, H. L. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.10.002 · Cited by 166 · see citing works
“One small molecule, the hamster pheromone dimethyl disulfide, exerts its effects through the vomeronasal system [ 62 ] but might arrive at the vomeronasal epithelium bound to a larger carrier molecule, aphrodisin [63].”
BackgroundSensory processing in the main and accessory olfactory systems: Comparisons and contrasts
Meredith, M. (1991) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(91)90258-7 · Cited by 155 · see citing works
Li, H. L., Roch, J., Sundsmo, M. P., Otero, D. A. C., Sisodia, S. S., Thomas, R. G., & Saitoh, T. (1997) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199705)32:5 · Cited by 56 · see citing works
Pfeiffer, C. A., & Johnston, R. E. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90020-5 · Cited by 125 · see citing works
Gu, G., Cornea, A., & Simerly, R. (2003) · The Journal of comparative neurology · doi:10.1002/cne.10677 · Cited by 103 · see citing works
Infanticide in rats: male strategy and female counter-strategy.
Mennella, J., & Moltz, H. (1988) · Physiology and Behavior · doi:10.1016/0031-9384(88)90254-5 · Cited by 101 · see citing works
Johnston, R. E. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb10592.x · Cited by 99 · see citing works
Male hamster sociosexual behaviors: effects of testosterone and its metabolites.
Powers, J., Bergondy, M. L., & Matochik, J. (1985) · Physiology and Behavior · doi:10.1016/0031-9384(85)90149-0 · Cited by 78 · see citing works
Kelliher, K. R., Liu, Y.-C. A., Baum, M. J., & Sachs, B. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00050-0 · Cited by 76 · see citing works
Aujard, F. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00206-0 · Cited by 73 · see citing works
Saito, T. R., & Moltz, H. (1986) · Physiology and Behavior · doi:10.1016/0031-9384(86)90215-5 · Cited by 74 · see citing works
Fewell, G. D., & Meredith, M. J. (2002) · Brain Research · doi:10.1016/s0006-8993(02)02613-6 · Cited by 68 · see citing works
Aphrodisin, an aphrodisiac lipocalin secreted in hamster vaginal secretions.
Briand, L., Trotier, D., & Pernollet, J. (2004) · Peptides · doi:10.1016/j.peptides.2003.10.026 · Cited by 64 · see citing works
“The importance of the accessory olfactory system for the copulatory responses of male hamsters to aphrodisin was assessed in animals that had their VNO removed [6].”
BackgroundBrouette-Lahlou, I., Godinot, F., & Vernet-Maury, E. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00334-5 · Cited by 62 · see citing works
A chemistry of mammalian pheromones
Singer, A. G. (1991) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(91)90261-3 · Cited by 66 · see citing works
Self-citationVomeronasal system, LHRH, and sex behaviour
Meredith, M. J., & Fernandez-Fewell, G. (1994) · Psychoneuroendocrinology · doi:10.1016/0306-4530(94)90048-5 · Cited by 57 · see citing works
The vomeronasal organ of Lemur catta
Smith, T. D., Muchlinski, M., Bhatnagar, K. P., Durham, E., Bonar, C., & Burrows, A. (2015) · American Journal of Primatology · doi:10.1002/ajp.22326 · Cited by 57
Odorant and pheromone binding by aphrodisin, a hamster aphrodisiac protein
Briand, L. V., Huet, J., Perez, V., Lenoir, G., Nespoulous, C., Boucher, Y., Trotier, D., & Pernollet, J. C. (2000) · FEBS Letters · doi:10.1016/s0014-5793(00)01719-1 · Cited by 59 · see citing works
Role of the vomeronasal system in intersexual attraction in female mice
Martínez‐Ricós, J., Agustín‐Pavón, C., Lanuza, E., & Martínez‐Garciá, F. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.002 · Cited by 54 · see citing works
Singer, A., Clancy, A., Macrides, F., & Agosta, W. (1984) · Physiology and Behavior · doi:10.1016/0031-9384(84)90385-8 · Cited by 55
Self-citationMendoza, A. S. (1993) · Annals of Anatomy · doi:10.1016/s0940-9602(11)80110-x · Cited by 53 · see citing works
Infanticide in the male rat: the role of the vomeronasal organ.
Mennella, J., & Moltz, H. (1988) · Physiology and Behavior · doi:10.1016/0031-9384(88)90087-x · Cited by 52 · see citing works
Role of the Vomeronasal Organ in Neonatal Offspring Recognition in Sheep1
Booth, K. K., & Katz, L. S. (2000) · Biology of Reproduction · doi:10.1095/biolreprod63.3.953 · Cited by 50 · see citing works
Johnston, R. E. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90163-v · Cited by 45 · see citing works
Johnston, R. E., & Peng, M. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00304-8 · Cited by 48 · see citing works
Sexual behavior in the female rat following removal of the vomeronasal organ.
Saito, T. R., & Moltz, H. (1986) · Physiology and Behavior · doi:10.1016/0031-9384(86)90135-6 · Cited by 44
Westberry, J. M., & Meredith, M. J. (2003) · Brain Research · doi:10.1016/s0006-8993(03)02535-6 · Cited by 38 · see citing works
ROLE OF THE VOMERONASAL INPUT IN MATERNAL BEHAVIOR
del Cerro, M. C. R. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00060-2 · Cited by 36 · see citing works
“1993), in vasopressinergic transmission (Bluthé and Dantzer, 1993), in courtship and in mating (Clancy et al. 1984).”
BackgroundClancy, A., Schoenfeld, T. A., Forbes, W. B., & Macrides, F. (1994) · Brain Research Bulletin · doi:10.1016/0361-9230(94)90060-4 · Cited by 41 · see citing works
Self-citationNatural ligands of hamster aphrodisin.
Briand, L., Blon, F., Trotier, D., & Pernollet, J. (2004) · Chemical Sensors · doi:10.1093/chemse/bjh044 · Cited by 38 · see citing works
“Aphrodisin stimulates the male copulatory behavior via the vomeronasal organ (Clancy et al., 1984; Kroner et al., 1996; Jang et al., 2001), but occurs in vaginal discharges before females reach fertility, suggesting another unknown function for aphrodisin (Mägert et al.”
BackgroundMacrides, F., Singer, A., Clancy, A., Goldman, B., & Agosta, W. (1984) · Physiology and Behavior · doi:10.1016/0031-9384(84)90383-4 · Cited by 36 · see citing works
Self-citationMendoza, A. S., & Szabó, K. (1988) · Brain Research · doi:10.1016/0165-3806(88)90030-2 · Cited by 35 · see citing works
The Chemistry of Vomeronasally Detected Pheromones: Characterization of an Aphrodisiac Protein a
Singer, A., Agosta, W. C., Clancy, A., & Macrides, F. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb36304.x · Cited by 35 · see citing works
Self-citationChemical properties of a female mouse pheromone that stimulates gonadotropin secretion in males.
Singer, A., Clancy, A., Macrides, F., Agosta, W. C., & Bronson, F. (1988) · Biology of Reproduction · doi:10.1095/biolreprod38.1.193 · Cited by 31 · see citing works
Self-citationBooth, K. K., & Webb, E. C. (2010) · Veterinary Medicine International · doi:10.4061/2011/305468 · Cited by 23 · see citing works
“Pheromones, which are detected by the vomeronasal organ [25], are known to influence a variety of animal activities from sexual maturation to maternal offspring recognition during nursing [3, 26–41].”
BackgroundMacrides, F., Clancy, A., Singer, A., & Agosta, W. (1984) · Physiology and Behavior · doi:10.1016/0031-9384(84)90382-2 · Cited by 30 · see citing works
Self-citationWestberry, J., & Meredith, M. (2003) · Chemical Sensors · doi:10.1093/chemse/28.3.191 · Cited by 29 · see citing works
“HVF has both sexual attractant (Johnston, 1974) and sexual stimulant qualities (Johnston, 1975) and contains components that can be classified as pheromones, largely acting via the VN system in intact males (Clancy et al., 1984).”
BackgroundSex Differences in Olfaction in Mammals
Dorries, K. (1992) · Springer eBooks · doi:10.1007/978-1-4612-2836-3_8 · Cited by 28 · see citing works
Stimulus access to the accessory olfactory system in the prenatal and perinatal rat.
Coppola, D. M., & Millar, L. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90257-7 · Cited by 26
Schaeffer, C., Roos, J., & Aron, C. (1986) · Hormones and Behavior · doi:10.1016/0018-506x(86)90034-6 · Cited by 26
Singer, A., Clancy, A., Macrides, F., & Agosta, W. (1984) · Physiology and Behavior · doi:10.1016/0031-9384(84)90384-6 · Cited by 26 · see citing works
Self-citationThavathiru, E., Jana, N., & De, P. (1999) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1999.00884.x · Cited by 24 · see citing works
Pieper, D., Newman, S., Lobocki, C., & Gogola, G. (1989) · Brain Research · doi:10.1016/0006-8993(89)90582-9 · Cited by 24
Eisthen, H., Wysocki, C., & Beauchamp, G. (1987) · Physiology and Behavior · doi:10.1016/0031-9384(87)90079-5 · Cited by 23
The Golden Hamster Aphrodisin Gene
Mägert, H., Cieslak, A., Alkan, O., Lüscher, B., Kauffels, W., & Forssmann, W. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.1.444 · Cited by 21 · see citing works
Chateau, D., Chabli, A., & Aron, C. (1987) · Physiology and Behavior · doi:10.1016/0031-9384(87)90232-0 · Cited by 21
Matsuoka, M., Mori, Y., HOSHINO, K., & Ichikawa, M. (1994) · Neuroscience Research · doi:10.1016/0168-0102(94)90142-2 · Cited by 19 · see citing works
Experiential and endocrine dependence of gonadotropin responses in male mice to conspecific urine.
Clancy, A., Singer, A., Macrides, F., Bronson, F., & Agosta, W. (1988) · Biology of Reproduction · doi:10.1095/biolreprod38.1.183 · Cited by 19 · see citing works
Self-citationMota‐Rojas, D., Marcet‐Rius, M., Freitas‐de‐Melo, A., Muns, R., Mora‐Medina, P., Domínguez-Oliva, A., & Orihuela, A. (2021) · Animals · doi:10.3390/ani11113092 · Cited by 22 · see citing works
“tions [43–46], and sexual [47–56] or aggressive behaviors [48].”
BackgroundWysocki, C., Beauchamp, G., Reidinger, R. R., & Wellington, J. (1985) · Journal of Chemical Ecology · doi:10.1007/bf01024105 · Cited by 18 · see citing works
Neuronal Development, Differentiation, and Plasticity in the Mammalian Vomeronasal System
Ichikawa, M. (1996) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.13.627 · Cited by 11 · see citing works
“Removal of the vomeronasal organ in hamsters results in a loss of responsiveness to the aphrodisiac stimulus of the highmolecular-weight fraction of the vaginal discharge (Clancy et al., 1984).”
BackgroundVomeronasal organ ablation elicits chemosensory dysfunction and abnormal behavior in mice
Liu, Y.-J., Zhang, J., Zhang, J.-H., Bao, W., & Liu, D.-Z. (2009) · Journal of Ethology · doi:10.1007/s10164-009-0180-x · Cited by 10 · see citing works
“VNO deficiency elicits a range of deficits in sexual behaviors in response to sex pheromones (Clancy et al. 1984; Meredith 1986; Pfeiffer and Johnston 1994; Keverne 2004; Brennan and Zufall 2006).”
BackgroundPerret, M., & Schilling, A. (1987) · Journal of Chemical Ecology · doi:10.1007/bf01880095 · Cited by 9 · see citing works
Mendoza, A., & Kühnel, W. (1991) · Acta Histochemica · doi:10.1016/s0065-1281(11)80273-4 · Cited by 9 · see citing works
Sánchez‐Criado, J. E., Mora, O. A., & Gallego, A. (1989) · Progress in sensory physiology · doi:10.1007/978-3-642-74058-9_5 · Cited by 10 · see citing works
Plastic effect of soiled bedding on the structure of synapses in rat accessory olfactory bulb
Ichikawa, M., Matsuoka, M., & Mori, Y. (1995) · Synapse · doi:10.1002/syn.890210203 · Cited by 8 · see citing works
Boehm, N., Lazarus, C., & Aron, C. (1991) · Physiology and Behavior · doi:10.1016/0031-9384(91)90428-q · Cited by 8
Sex separation unveils the functional plasticity of the vomeronasal organ in rabbits
Villamayor, P., Gullón, J., Quintela, L., Sánchez-Quinteiro, P., Martínez, P., & Robledo, D. (2022) · bioRxiv · doi:10.3389/fnmol.2022.1034254 · Cited by 7 · see citing works
“, 1999) and it is detected by the male VNS eliciting copulatory behaviour in male hamster (Clancy et al., 1984; Kroner et al., 1996; Jang et al., 2001; Briand et al., 2004a).”
BackgroundContreras, C. M., Gutiérrez‐García, A. G., & Molina‐Jiménez, T. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.05.037 · Cited by 9 · see citing works
Sublingual plicae (anterior processes) are not necessary for garter snake vomeronasal function.
Halpern, M., & Borghjid, S. (1997) · Journal of Comparative Psychology · doi:10.1037/0735-7036.111.3.302 · Cited by 7
Recent Advances in Reproductive Technologies
Honaramooz, A., Schlatt, S., Orwig, K. E., & Kim, N. H. (2011) · Veterinary Medicine International · doi:10.4061/2011/915031 · Cited by 6 · see citing works
Liu, Y., Wang, D., Sun, L.-X., Zhang, J.-H., & Zhang, J.-X. (2010) · doi:10.1093/czoolo/56.6.800 · Cited by 6
“…mostly on vaginal secretions and not on secretions of the flank gland, resulting in the discovery of several putative pheromones such as dimethyl disulfide and aphrodin (Singer et al., 1977, 1984; Clancy et al., 1984; Singer and Macrides, 1990; Petrulis and Johnston, 1995; Briand et al., 2004).”
BackgroundTestosterone and chemosensory detection in male Syrian hamster.
Peters, K. D., Hom, S. M., & Wood, R. I. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.04.004 · Cited by 6
On the persistence of mouse urine odour to human observers: a review
Kwak, J., Jackson, M., Faranda, A. P., Osada, K., Tashiro, T., Mori, K., Quan, Y., Voznessenskaya, V., & Preti, G. (2016) · Flavour and Fragrance Journal · doi:10.1002/ffj.3316 · Cited by 6 · see citing works
Lipocalycins Associated with Mammalian Pheromones
Singer, A., & Macrides, F. (1992) · Springer eBooks · doi:10.1007/978-1-4757-9655-1_19 · Cited by 6 · see citing works
Self-citationHormones and Neurotransmitters in the Mammalian Olfactory System a
Macrides, F., Schoenfeld, T. A., Clancy, A., Kumar, M. S., & Kream, R. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb36294.x · Cited by 5 · see citing works
Self-citationProgress in Sensory Physiology 9
Shimazu, H. (1989) · Progress in Sensory Physiology · doi:10.1007/978-3-642-74058-9 · Cited by 5 · see citing works
Signaling in the Mammalian Vomeronasal Organ
Wekesa, K. S. (2012) · Biochemistry & Physiology Open Access · doi:10.4172/2168-9652.1000e110 · Cited by 2 · see citing works
“For example, impaired sexual behavior toward females has been reported in male mice after VNO lesions [42] whereas no such deficits were reported in TRPC2-/- mice [33,34,41].”
BackgroundVomeronasal organ and the accessory olfactory system
Whitten, W. (1985) · doi:10.1016/0168-1591(85)90021-8 · Cited by 3
Is the Mouse Vomeronasal Organ a Sex Pheromone Receptor
Hatanaka, T. (1992) · doi:10.1007/978-1-4757-9655-1_5 · Cited by 3
The stimulus control of sexual incentive motivation
Ågmo, A. (2007) · Elsevier eBooks · doi:10.1016/b978-012370590-7/50004-9
Li, C.-S., Kubie, J., & Halpern, M. (2005) · doi:10.1007/0-387-25160-x_29 · Cited by 1
“All of these behavioral responses to large molecular weight, biologically significant compounds or substances require a functional vomeronasal system (Beauchamp et al., 1982, 1985; Kubie and Halpem, 1979; Clancy et al., 1984 ).”
BackgroundDETERMINATION OF APHRODISIN GENE OF SYRIAN HAMSTER BY MOLECULAR TECHNIQUE
Khan, M., & De, P. (2012) · doi:10.3329/bjvm.v8i2.11202
“…pheromone that is deposited upon the snout and tongue of the male by contact during normal chemosensory investigation of the female’s vaginal discharge by the male hamster, and it is probably transported in the nasal mucus to chemoreceptors in the male’s vomeronasal organ (Clancy et al., 1984).”
Background
- Authors
- Clancy, A. N., Macrides, F., Singer, A. G., & Agosta, W. C.
- Affiliations
- Rockefeller University (US)
- Corresponding author
- Macrides, Foteos
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 1984-10
- Volume
- 33
- Issue
- 4
- Pages
- 653-660
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W1984568343
- Cited by
- 83
- References
- 0
- Citations by year
- 2022: 1 · 2021: 1 · 2016: 1 · 2014: 1 · 2013: 2 · 2012: 2
- FWCI
- 4.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- vomeronasal organ, accessory olfactory system, male hamsters, mating behavior, vaginal discharge, high molecular weight fraction, accessory olfactory bulb, pheromonal communication, intromission, gustatory processing, olfactory system
- MeSH terms
- Animals, Copulation, Exploratory Behavior, Female, Cricetinae, Male, Mesocricetus, Olfactory Mucosa, Pheromones, Sex Attractants, Sexual Behavior, Animal, Smell, Vagina
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