Pheromonally induced release of luteinizing hormone in male mice: involvement of the vomeronasal system
Open accessAbstract
Evidence has accumulated demonstrating that the vomeronasal (accessory olfactory) system mediates intraspecific chemosensory communication in several mammals. For example, the neuroendocrine effects of priming pheromones in females and the behavioral responses to signaling pheromones in males are disrupted in mice with damage to the vomeronasal system. The experiment reported here examined the potential involvement of the vomeronasal system in the neuroendocrine reflexes observed in male mice following exposure to female and chemosensory stimuli. Excision of the vomeronasal organ (VNO) or sham VNO ablation was performed on sexually experienced males. Next, consecutive blood samples were withdrawn through chronic, intracardiac cannulas while the males were exposed to female mouse urine and then to an ovariectomized female. Plasma levels of luteinizing hormone (LH) were measured in the sequential samples by radioimmunoassay. Removal of the VNO did not affect the spontaneous pattern of episodic LH release that is characteristic of male mice. Reflexive release of LH following the urine stimulus was blocked in males lacking the VNO, but the female stimulus did cause LH responses in these mice. Our results therefore demonstrate that the VNO mediates pheromonally induced release of LH in male mice and that additional cues which emanate from behaving females also effectively stimulate a hormonal response in sexually experienced males.
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The increase in serum luteinizing hormone and testosterone when male mice and hamsters are exposed to chemosensory stimuli from females appears to be absolutely dependent on vomeronasal integrity.
“The increase in serum luteinizing hormone and testosterone when male mice and hamsters are exposed to chemosensory stimuli from females appears to be absolutely dependent on vomeronasal integrity (Coquelin et al., 1984;Pfeiffer and Johnston, 1994).”
From Human Vomeronasal Organ Function: A Critical Review of Best and Worst Cases (2001) · cites this paper as Coquelin et al., 1984
The Results (page not provided) show that removing the vomeronasal organ greatly reduced LH responses to female urine in male mice. But some mice without the organ still responded to urine, and most responded to a freely behaving female, so the paper does not establish absolute dependence for all female stimuli. It reports a testosterone finding from another mouse study but does not study testosterone or hamsters itself. (LLM, conf=0.90)
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Cites
Introduction to Statistical Analysis.
Latshaw, V. V., Dixon, W. J., & Massey, F. J. (1957) · American Mathematical Monthly · doi:10.2307/2309989 · Cited by 5,072 · see citing works
Biology of the Laboratory Mouse
(1941) · JAMA · doi:10.1001/jama.1941.02820440081034 · Cited by 805 · see citing works
Neurobehavioral evidence for the involvement of the vomeronasal system in mammalian reproduction.
Wysocki, C. (1979) · Neuroscience and Biobehavioral Reviews · doi:10.1016/0149-7634(79)90015-0 · Cited by 478 · see citing works
Pheromones and Reproduction in Mammals
(1983) · Elsevier eBooks · doi:10.1016/b978-0-12-710780-6.x5001-8 · Cited by 416 · cited 1× · see citing works
“The substances released by mammals often profoundly alter the reproductive processes of the individuals exposed to the stimuli (see reviews in Doty, 1976, and Vandenbergh, 1983).”
BackgroundGraham, J. M., & Desjardins, C. (1980) · Science · doi:10.1126/science.7434016 · Cited by 268 · cited 1× · see citing works
“In male rats, an olfactory cue from a decidedly non-female originodor of wintergreen-has been shown by Graham and Desjardins (1980) to cause a neuroendocrine reflex when the conditioned stimulus previously had been associated with females in a sexual context.”
BackgroundStrange Females Increase Plasma Testosterone Levels in Male Mice
Macrides, F., Bartke, A., & Dalterio, S. L. (1975) · Science · doi:10.1126/science.1162363 · Cited by 184 · cited 1× · see citing works
“Mediation of primer responses by the vomeronasal system in male mice is likely, given the neuroendocrine reflexes that are stimulated by females or by the urine of females (Macrides et al., 1975; Maruniak and Bronson, 1976).”
BackgroundSelf-citationSexual behavior and aggression in male mice: involvement of the vomeronasal system
Clancy, A., Coquelin, A., Macrides, F., Gorski, R., & Noble, E. P. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-09-02222.1984 · Cited by 180 · cited 8× · see citing works
“Thus, excision of the VNO from 10 males virtually eliminated its afferent projections to the accessory olfactory bulb, whereas the projections of the VNO remained intact in the 12 mice receiving sham surgeries (see Clancy et al., 1984, for further details).”
BackgroundMethodInfluentialSelf-citationRussell, E. S., & Bernstein, S. E. (1966) · The Mouseion at the JAXlibrary (Jackson Laboratory) · Cited by 176 · see citing works
Bellringer, J. F., Pratt, H. P. M., & Keverne, E. B. (1980) · Reproduction · doi:10.1530/jrf.0.0590223 · Cited by 166 · cited 2× · see citing works
“This function of the vomeronasal system in male ,mice seems analogous to its clearly documented role in the responses of female mice to pheromones (Reynolds and Keverne, 1979; Bellringer et al., 1980; Kaneko et al., 1980).”
BackgroundThe vomeronasal organ: Primary role in mouse chemosensory gender recognition
Wysocki, C. J., Nyby, J., Whitney, G., Beauchamp, G. K., & Katz, Y. (1982) · Physiology & Behavior · doi:10.1016/0031-9384(82)90021-x · Cited by 163 · cited 1× · see citing works
“Furthermore, the vomeronasal system is involved in the ultrasonic vocalizations evoked in male mice by female odors and in the agonistic and copulatory behaviors of male mice, all of which are responses to signaling pheromones (Wysocki et al., 1982; Clancy et al., 1984).”
BackgroundLuteinizing hormone and testosterone secretion in young and old male mice
Coquelin, A. W., & Desjardins, C. D. (1982) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1982.243.3.e257 · Cited by 161 · cited 4× · see citing works
“Transfusion of this substitute previously has been documented to sustain mice during extended periods of blood sampling (Coquelin and Bronson, 1981; Coquelin and Desjardins, 1982).”
BackgroundMethodInfluentialSelf-citationA Citrate-Phosphate-Dextrose Solution for the Preservation of Human Blood
Gibson, J. G., Rees, S. B., McManus, T. J., & Scheitlin, W. A. (1957) · American Journal of Clinical Pathology · doi:10.1093/ajcp/28.6.569 · Cited by 157 · cited 1× · see citing works
“T. J. McManus. and W. A. Scheitlin (1957) A citrate-phosphate-dextrose solution for the preservation of human blood.”
BackgroundBronson, F. H., & Desjardins, C. (1974) · Endocrinology · doi:10.1210/endo-94-6-1658 · Cited by 143 · see citing works
The effect of olfactory stimuli on the agonistic behaviour of laboratory mice.
Mackintosh, J. H., & Grant, E. C. (2010) · Zeitschrift für Tierpsychologie · doi:10.1111/j.1439-0310.1966.tb01614.x · Cited by 133 · see citing works
Reynolds, J., & Keverne, E. B. (1979) · Reproduction · doi:10.1530/jrf.0.0570031 · Cited by 122 · see citing works
Gonadotropic Responses of Male Mice to Female Urine
MARUNIAK, J. A., & Bronson, F. H. (1976) · Endocrinology · doi:10.1210/endo-99-4-963 · Cited by 115 · cited 2× · see citing works
“Mediation of primer responses by the vomeronasal system in male mice is likely, given the neuroendocrine reflexes that are stimulated by females or by the urine of females (Macrides et al., 1975; Maruniak and Bronson, 1976).”
BackgroundMethodKaneko, N., Debski, E. A., Wilson, M. C., & Whitten, W. K. (1980) · Biology of Reproduction · doi:10.1095/biolreprod22.4.873 · Cited by 105 · cited 3× · see citing works
“Interrupting vomeronasal afferents eliminates the acceleration of puberty in juvenile females, the suppression of estrous cyclicity in females housed in groups, and the blockade of pregnancy by exposure to unfamiliar males, all of which are responses to priming pheromones in mice (Reynolds and Keverne, 1979; Bellringe…”
BackgroundMale Vomeronasal Organ Mediates Female-Induced Testosterone Surges in Mice
Wysocki, C. J., Katz, Y., & Bernhard, R. (1983) · Biology of Reproduction · doi:10.1095/biolreprod28.4.917 · Cited by 99 · cited 2× · see citing works
“In fact, ablation of the VNO in male mice recently has been reported to prevent the elevation of circulating testosterone levels which follows presentation of an anesthetized female (Wysocki et al., 1983).”
BackgroundResultScalia, F., & Winans, S. S. (1976) · Elsevier eBooks · doi:10.1016/b978-0-12-221250-5.50007-3 · Cited by 76 · cited 2× · see citing works
“From sensory receptors in the vomeronasal organ (VNO), the vomeronasal system projects multisynaptically to the medial amygdaloid nucleus and posteromedial cortical amygdaloid area, the bed nucleus of the stria terminalis, the medial preoptic area, and the ventromedial nucleus of the hypothalamus (Scalia and Winans, 1…”
BackgroundCoquelin, A., & Bronson, F. H. (1980) · Endocrinology · doi:10.1210/endo-106-4-1224 · Cited by 74 · cited 7× · see citing works
“Thus, although this result does not invalidate the basic concept of an all-or-nothing episode of LH release (Coquelin and Bronson, 1980), the durations of individual secretory episodes or hormonal disappearance rates may be influenced to some extent by sensory and/or behavioral variables (cf.…”
BackgroundMethodInfluentialSelf-citationRadioimmunoassay of Mouse Luteinizing and Follicle Stimulating Hormones
Beamer, W. G., MURR, S. M., & Geschwind, I. I. (1972) · Endocrinology · doi:10.1210/endo-90-3-823 · Cited by 62 · see citing works
Preparation and Properties of a Heat-Treated Human Plasma Protein Fraction
Hink, J. H., HIDALGO, J., Seeberg, V. P., & Johnson, F. F. (1957) · Vox Sanguinis · doi:10.1111/j.1423-0410.1957.tb03452.x · Cited by 55 · cited 2× · see citing works
“…experienced males to release LH reliably after exposure to a behaviorally active female, but the presence of the VNO is important for the urine of females to evoke the hormonal response. sodium heparin and 5% citrate/phosphate/dextrose solution added (Gibson et al., 1957, 1961; Hink et al., 1957).”
BackgroundEpisodic Release of Luteinizing Hormone in Male Mice: Antagonism by a Neural Refractory Period*
Coquelin, A. W., & Bronson, F. H. (1981) · Endocrinology · doi:10.1210/endo-109-5-1605 · Cited by 34 · cited 2× · see citing works
“Transfusion of this substitute previously has been documented to sustain mice during extended periods of blood sampling (Coquelin and Bronson, 1981; Coquelin and Desjardins, 1982).”
BackgroundSelf-citation
Flagged first, then by citations
1 of the 24 references couldn’t be matched to a known paper.
Research works printed but not linked: 3
- Bronson, F. H. (1974) Pheromonal influences on reproductive activities in rodents. In Pheromones, M. C. Birch, ed., pp. 344-365, Elsevier, New York.
- Dixon, W. J., and F. J. Massey, Jr. (1969) Introduction to Statistical Anal&s. Ed. 3. McGraw-Hill. New York.
- Doty, 6. i. (1976) Mammalian'Olfaction, Reproductive Processes, and Bkhauior, Academic Press, Inc., New York.
Cited by
Sorted by citations
Olfactory Inputs to Hypothalamic Neurons Controlling Reproduction and Fertility
Yoon, H., Enquist, L. W., & Dulac, C. G. (2005) · Cell · doi:10.1016/j.cell.2005.08.039 · Cited by 435 · see citing works
“Experimental Design Chemosensory inputs have been reported in a number of rodent species to modulate the activity of LHRHexpressing neurons (Coquelin et al., 1984; Richardson et al., 2004).”
BackgroundFeedback Loops Link Odor and Pheromone Signaling with Reproduction
Boehm, U., Zou, Z., & Buck, L. B. (2005) · Cell · doi:10.1016/j.cell.2005.09.027 · Cited by 331 · see citing works
Membrane and synaptic properties of identified neurons in the olfactory bulb
Mori, K. (1987) · Progress in Neurobiology · doi:10.1016/0301-0082(87)90024-4 · Cited by 320 · see citing works
Steyn, F. J., Wan, Y., Clarkson, J., Veldhuis, J. D., Herbison, A. E., & Chen, C. (2013) · Endocrinology · doi:10.1210/en.2013-1502 · Cited by 304 · see citing works
“Seminal studies by Coquelin and coworkers (8, 9) and Kokoris et al (10) were the first to define the pulsatile patterns of LH secretion in the adult male mouse, and subsequent studies have provided similar information for adult female mice (11, 12).”
BackgroundStructure and function of the vomeronasal organ
Döving, K. B., & Trotier, D. (1998) · Journal of Experimental Biology · doi:10.1242/jeb.201.21.2913 · Cited by 293 · 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
“The increase in serum luteinizing hormone and testosterone when male mice and hamsters are exposed to chemosensory stimuli from females appears to be absolutely dependent on vomeronasal integrity (Coquelin et al., 1984; Pfeiffer and Johnston, 1994).”
BackgroundTestosterone release and social context: When it occurs and why
Gleason, E. D., Fuxjager, M. J., Oyegbile, T. O., & Marler, C. A. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.04.009 · Cited by 268 · see citing works
Wersinger, S. R., & Rissman, E. F. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00418.x · Cited by 198 · see citing works
Leptin signaling and circuits in puberty and fertility
Elias, C. F., & Purohit, D. (2012) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1095-1 · Cited by 190 · see citing works
“In response to opposite sex odors, males and females from different species exhibit increased circulating levels of gonadotropins and sex steroids [26, 85, 180, 214, 223, 264].”
BackgroundSexual behavior and aggression in male mice: involvement of the vomeronasal system
Clancy, A., Coquelin, A., Macrides, F., Gorski, R., & Noble, E. P. (1984) · Journal of Neuroscience · doi:10.1523/jneurosci.04-09-02222.1984 · Cited by 180 · see citing works
“…blocks a variety of pheromonally mediated responses in mice including pregnancy block (Bellringer et al., 1980), puberty acceleration (Kaneko et al., 1980), estrus suppression (Reynolds and Keverne, 1979), and the female-elicited LH/T surge in males (Wysocki et al., 1983; Coquelin et al., 1984).”
BackgroundResultInfluentialSelf-citationFernandez-Fewell, G. D., & Meredith, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03643.1994 · Cited by 176 · see citing works
“Given the evidence for an LH response in males exposed to females (Wysocki et al., 1983; Coquelin et al., 1984) it seems more likely that there is activation, but at too low a level to be visible as an increase in Fos expression.”
BackgroundTHE OSTEOLOGY OF RHOMBOMYLUS (MAMMALIA, GLIRES): IMPLICATIONS FOR PHYLOGENY AND EVOLUTION OF GLIRES
Meng, J., Hu, Y., & Li, C. (2003) · Bulletin of the American Museum of Natural History · doi:10.1206/0003-0090(2003)275 · Cited by 171 · see citing works
Consequences of removing the vomeronasal organ.
Wysocki, C., & Lepri, J. (1991) · Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(91)90265-7 · Cited by 167 · see citing works
Conrad, P., Wu, F., & Schacher, S. (1999) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199905)39:2 · Cited by 37 · see citing works
Chemosignals, hormones and mammalian reproduction
Petrulis, A. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.03.011 · Cited by 142 · see citing works
“VNO removal eliminates or reduces LH/androgen surges in both sexually experienced and naïve males in response to female chemosignals, but not to the female herself; damage to MOE is without effect (Coquelin et al., 1984; Pfeiffer and Johnston, 1994; Wysocki et al., 1983).”
Hypothalamic Sites of Leptin Action Linking Metabolism and Reproduction
Donato, J., Cravo, R. M., Frazão, R., & Elias, C. F. (2010) · Neuroendocrinology · doi:10.1159/000322472 · Cited by 141 · see citing works
The “male effect” in sheep and goats: a review of the respective roles of the two olfactory systems
Gelez, H., & Fabre‐Nys, C. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.05.002 · Cited by 140 · 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
Satou, M. (1990) · Progress in Neurobiology · doi:10.1016/0301-0082(90)90004-z · Cited by 123 · see citing works
Sensory 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
Halem, H. A., Baum, M. J., & Cherry, J. A. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-07-02474.2001 · Cited by 108 · see citing works
“For example, in male mice, exposure to female pheromones facilitates luteinizing hormone secretion (Johnston and Bronson, 1982; Coquelin et al., 1984) and stimulates ultrasonic vocalizations (Nyby et al.”
BackgroundDaikoku‐Ishido, H., Okamura, Y., Yanaihara, N., & Daikoku, S. (1990) · Developmental Biology · doi:10.1016/0012-1606(90)90087-y · Cited by 108 · see citing works
Vomeronasal, Olfactory, Hormonal Convergence in the Brain: Cooperation or Coincidence? <sup>a</sup>
MEREDITH, M. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb10593.x · Cited by 121 · see citing works
Estrogen Receptor α Influences Socially Motivated Behaviors
Imwalle, D. B., Scordalakes, E. M., & Rissman, E. F. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1837 · Cited by 95 · see citing works
Sexual Differentiation of the Neuroendocrine Mechanisms Regulating Mate Recognition in Mammals
Bakker, J. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01036.x · Cited by 90 · see citing works
Terminal nerve damage impairs the mating behavior of the male hamster.
Wirsig, C., & Leonard, C. (1987) · Brain Research · doi:10.1016/0006-8993(87)90454-9 · Cited by 78 · see citing works
McGivern, R. F., Sokol, R. Z., & Berman, N. (1991) · Toxicology and Applied Pharmacology · doi:10.1016/s0041-008x(05)80003-1 · Cited by 81 · see citing works
Evolution of the Amygdala in Vertebrates
Martínez‐Garciá, F., Novejarque, A., & Lanuza, E. (2007) · Elsevier eBooks · doi:10.1016/b0-12-370878-8/00139-7 · Cited by 80 · see citing works
Vomeronasal organ removal and female mouse aggression: The role of experience
Bean, N. J., & Wysocki, C. J. (1989) · Physiology & Behavior · doi:10.1016/0031-9384(89)90209-6 · Cited by 79 · see citing works
The combined role of the main olfactory and vomeronasal systems in social communication in mammals
Kelliher, K. R. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.08.012 · Cited by 78 · see citing works
“;) an effect that appears primarily (or absolutely in the case of hamsters) mediated by vomeronasal organ (Wysocki et al., 1983; Coquelin et al., 1984; Pfeiffer and Johnston, 1994).”
BackgroundMediation of male mouse urine marking and aggression by the vomeronasal organ
MARUNIAK, J. A., Wysocki, C. J., & Taylor, J. A. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90300-8 · Cited by 75 · see citing works
Petrulis, A., Peng, M., & Johnston, R. E. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00259-5 · Cited by 74 · see citing works
Processing by the main olfactory system of chemosignals that facilitate mammalian reproduction
Baum, M. J., & Cherry, J. A. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.06.003 · Cited by 73 · see citing works
Aujard, F. (1997) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00206-0 · Cited by 73 · see citing works
Mouse vomeronasal organ: Effects on chemosignal production and maternal behavior
Lepri, J. J., Wysocki, C. J., & Vandenbergh, J. G. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90416-0 · Cited by 71 · see citing works
Mori, K., Imamura, K., Fujita, S. C., & Obata, K. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90018-2 · Cited by 71 · see citing works
Inhibition Shapes Sex Selectivity in the Mouse Accessory Olfactory Bulb
Hendrickson, R. C., Krauthamer, S., Essenberg, J. M., & Holy, T. E. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2715-08.2008 · Cited by 69 · see citing works
“This hormonal surge may (Coquelin et al., 1984) or may not (Pfeiffer and Johnston, 1994) rely exclusively on the accessory olfactory system.”
Kumar, A., Dudley, C. A., & Moss, R. L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-j0003.1999 · Cited by 68 · see citing works
“The publication date is the date of posting online at www.jneurosci.org. http://www.jneurosci.org/cgi /content/full /3549 in luteinizing hormone and testosterone (Wysocki et al., 1983; Coquelin et al., 1984) and to promote copulatory behavior (Clancy et al., 1984).”
BackgroundA 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
Dudley, C. A., & Moss, R. L. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00711-8 · Cited by 63 · see citing works
Clancy, A. N., Macrides, F., Singer, A. G., & Agosta, W. C. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90386-x · Cited by 83 · see citing works
Self-citationNeuroanatomical pathways linking vision and olfaction in mammals
Cooper, H. M., Parvopassu, F., Herbin, M., & Magnin, M. (1994) · Psychoneuroendocrinology · doi:10.1016/0306-4530(94)90046-9 · Cited by 63 · see citing works
Neural pathways involved in the endocrine response of anestrous ewes to the male or its odor
Gelez, H., & Fabre‐Nys, C. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.02.066 · Cited by 61 · see citing works
Schwanzel-Fukuda, M., Garcia, M. S., Morrell, J., & Pfaff, D. (1987) · The Journal of comparative neurology · doi:10.1002/cne.902550207 · Cited by 60 · see citing works
The functionality of the human vomeronasal organ (VNO): Evidence for steroid receptors
Berliner, D. L., Monti-Bloch, L., Jennings-White, C., & Diaz-Sanchez, V. (1996) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/0960-0760(96)00062-3 · Cited by 87 · see citing works
Female odors stimulate CART neurons in the ventral premammillary nucleus of male rats
Cavalcante, J. C., Bittencourt, J. C., & Elias, C. F. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.03.032 · Cited by 58 · see citing works
Vomeronasal 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
Samuelsen, C. L., & Meredith, M. J. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.09.030 · Cited by 58 · see citing works
Chiropteran vomeronasal complex and the interfamilial relationships of bats
Wible, J. R., & Bhatnagar, K. P. (1996) · Journal of Mammalian Evolution · doi:10.1007/bf02077447 · Cited by 55 · see citing works
“Among mammals, the VNO is widely distributed (Broom, 1897; Wysocki, 1979) and sensory input from it has been implicated in the control of sexual behavior (Coquelin et al., 1984; Halpern, 1987; Meredith and Fernfindez-Fewell, 1994).”
BackgroundFernandez-Fewell, G., & Meredith, M. J. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(94)00276-b · Cited by 52 · see citing works
Mendoza, A. S. (1993) · Annals of Anatomy · doi:10.1016/s0940-9602(11)80110-x · Cited by 53 · 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
Men Smelling Women: Null Effects of Exposure to Ovulatory Sweat on Men's Testosterone
Roney, J. R., & Simmons, Z. L. (2012) · Evolutionary Psychology · doi:10.1177/147470491201000404 · Cited by 48 · see citing works
Wysocki, C., Beauchamp, G., Reidinger, R. R., & Wellington, J. (1985) · Journal of Chemical Ecology · doi:10.1007/bf01024105 · Cited by 18 · see citing works
“, 1980), modulation of hormone levels (Wysocki et al., 1983; Coquelin et al., 1984), maternal behavior (Fleming et al.”
Johnston, R. E., & Peng, M. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00304-8 · Cited by 48 · see citing works
Alexander, B. M., Stellflug, J. N., Rose, J. D., Fitzgerald, J. A., & Moss, G. E. (1999) · Journal of Animal Science · doi:10.2527/1999.7771869x · Cited by 47 · see citing works
Das vomeronasale Organ des Menschen
Knecht, M., Witt, M., Abolmaali, N., Hüttenbrink, K., & Hummel, T. R. (2003) · Der Nervenarzt · doi:10.1007/s00115-003-1573-7 · Cited by 45 · see citing works
Sexual Modulation of Testosterone: Insights for Humans from Across Species
Goldey, K. L., & van Anders, S. M. (2014) · Adaptive Human Behavior and Physiology · doi:10.1007/s40750-014-0005-1 · Cited by 45 · see citing works
“However, while removal of the vomeronasal organ in male mice blocked LH responses to female urine, LH still responded to an interaction with a female, suggesting that visual and/or auditory components of female behavior can compensate for the lack of pheromonal stimuli (Coquelin et al. 1984).”
BackgroundJansen, H. T., Iwamoto, G. A., & Jackson, G. L. (1998) · Brain Research Bulletin · doi:10.1016/s0361-9230(97)00279-7 · Cited by 45 · see citing works
The Septal Region and Social Behavior
Sheehan, T. P., & Numan, M. (2000) · Springer eBooks · doi:10.1007/978-1-4612-1302-4_8 · Cited by 44 · see citing works
The Ventral Premammillary Nucleus Links Metabolic Cues and Reproduction
Donato, J., & Elias, C. F. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00057 · Cited by 43 · see citing works
“In response to conspecific odors, males and females of different species exhibit increased circulating levels of gonadotropins and sex steroids (Maruniak and Bronson, 1976; Kamel et al., 1977; Beltramino and Taleisnik, 1983; Coquelin et al., 1984).”
BackgroundKelliher, K. R., & Wersinger, S. R. (2009) · ILAR Journal · doi:10.1093/ilar.50.1.28 · Cited by 40 · see citing works
Anand, S., Losee-Olson, S. H., Turek, F. W., & Horton, T. H. (2002) · Endocrinology · doi:10.1210/endo.143.6.8839 · Cited by 39 · see citing works
“LH and T secretion as well as behavioral changes have been shown to be induced in male mice, sheep, and Golden hamsters by exposure to conspecific females (16, 17, 19).”
BackgroundAggarwal, S., Tang, C., Sing, K., Kim, H. W., Millar, R. P., & Tello, J. A. (2018) · Neuroendocrinology · doi:10.1159/000496106 · Cited by 39 · see citing works
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
“hormone levels (Coquelin et al. 1984; Pfeiffer and Johnston 1994), in aggression (Novikov,”
BackgroundPfeiffer, C. A., & Johnston, R. E. (1992) · Hormones and Behavior · doi:10.1016/0018-506x(92)90048-z · Cited by 37 · see citing works
Mendoza, A. S., & Szabó, K. (1988) · Brain Research · doi:10.1016/0165-3806(88)90030-2 · Cited by 35 · see citing works
Odor here, odor there: chemosensation and reproductive function
Keverne, E. B. (2005) · Nature Neuroscience · doi:10.1038/nn1205-1637 · Cited by 34 · 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-citationUltrasonic vocalizations by adult prairie voles,Microtus ochrogaster
Lepri, J. J., Theodorides, M. L., & Wysocki, C. J. (1988) · Cellular and Molecular Life Sciences · doi:10.1007/bf01941736 · Cited by 33 · see citing works
Intracerebroventricular LHRH relieves behavioral deficits due to vomeronasal organ removal
Meredith, M. J., & Howard, G. (1992) · Brain Research Bulletin · doi:10.1016/0361-9230(92)90011-l · Cited by 33 · see citing works
Gelez, H., & Fabre‐Nys, C. (2006) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:2006021 · Cited by 30 · see citing works
“For example, the destruction of the VNO impairs the surge of LH and testosterone elicited by female odor in both sexually naive and experienced males [55,56].”
BackgroundThe vomeronasal system in mice: From the nose to the hypothalamus- and back!
Boehm, U. (2006) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2006.04.013 · Cited by 31 · see citing works
Chemical 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-citationDistribution of the neuronal inputs to the ventral premammillary nucleus of male and female rats
Cavalcante, J. C., Bittencourt, J. C., & Elias, C. F. (2014) · Brain Research · doi:10.1016/j.brainres.2014.07.034 · Cited by 29 · see citing works
Johnston, R., & delBarco‐Trillo, J. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00011-5 · Cited by 28 · see citing works
“In male mammals the VNO is also important in modulation of hormones; for example, lesions of the VNO or the AOB eliminate the following effects: (1) an increase in LH and testosterone in male mice after exposure to female mice or their odors (Coquelin and Bronson, 1980; Coquelin et al., 1984) and (2) increases in test…”
BackgroundLoi, P. K., & Tublitz, N. J. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000515)420:4 · Cited by 38 · 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-citationVomeronasal organ: electrical stimulation activates Fos in mating pathways and in GnRH neurons
Meredith, M. J., & Fewell, G. D. (2001) · Brain Research · doi:10.1016/s0006-8993(01)03153-5 · Cited by 26 · see citing works
Blake, C. B., & Meredith, M. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.05.056 · Cited by 25 · see citing works
“Conspecific chemosignals are known to induce testosterone surges in hamsters (Macrides et al., 1974) and mice (Coquelin et al., 1984), an effect dependent on an intact vomeronasal organ in both species (Pfeiffer and Johnston, 1994; Coquelin et al., 1984; Wysocki et al., 1983).”
Luteinizing Hormone‐Releasing Hormone in the Vomeronasal System and Terminal Nerve of the Hamster a
Lehman, M. N., Newman, S., & Silverman, A. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb36300.x · Cited by 28 · see citing works
Dulka, J. G., & Stacey, N. E. (1991) · Journal of Experimental Zoology · doi:10.1002/jez.1402570212 · Cited by 25 · see citing works
The Mammalian Vomeronasal System: Its Role in Learning and Social Behaviors
Wysocki, C. J., Bean, N. J., & Beauchamp, G. K. (1986) · Springer eBooks · doi:10.1007/978-1-4613-2235-1_36 · Cited by 24 · see citing works
Booth, 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].”
BackgroundSaito, H., Mimmack, M. L., Keverne, E. B., Kishimoto, J., & Emson, P. C. (1998) · Molecular Brain Research · doi:10.1016/s0169-328x(98)00183-1 · Cited by 23 · see citing works
Russell, N. V., Ogaga-Mgbonyebi, E. V., Habteab, B. S., Dunigan, A. I., Tesfay, M. A., & Clancy, A. N. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.04.017 · Cited by 22 · see citing works
Self-citationBeny, Y., & Kimchi, T. (2016) · Genes Brain & Behavior · doi:10.1111/gbb.12320 · Cited by 21 · see citing works
“…of cop-ulatory behavioral and physiological responses in sexually naïve males, for example the rapid elevation of circulating luteinizing hormone (Coquelin et al. 1984; Gleason et al. 2009; Goldey & van Anders 2014) and testosterone levels (Amstislavskaya et al. 2013; Gleason et al. 2009; Swaney…”
BackgroundGore, A. C., Wersinger, S. R., & Rissman, E. F. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00578.x · Cited by 22 · see citing works
Blissitt, M. J., Bland, K. P., & Cottrell, D. F. (1990) · Applied Animal Behaviour Science · doi:10.1016/0168-1591(90)90128-z · Cited by 21 · see citing works
Sex-specific Responses to Urinary Chemicals by the Mouse Vomeronasal Organ
Thompson, R. N. (2004) · Chemical Senses · doi:10.1093/chemse/bjh076 · Cited by 21 · see citing works
“For example, in male mice, exposure to female pheromones facilitates luteinizing hormone secretion (Johnston and Bronson, 1982; Coquelin et al., 1984) and stimulates ultrasonic vocalizations (Nyby et al., 1979), whereas exposure to male pheromones elicits inter-male aggressive behavior (Guillot and…”
BackgroundMota‐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
Olfactory Systems in Mate Recognition and Sexual Behavior
Keller, M., Pillon, D., & Bakker, J. (2010) · Vitamins and hormones · doi:10.1016/s0083-6729(10)83014-6 · Cited by 16 · see citing works
“…indirectly) to GnRH neurons (Boehm et al., 2005), and various experiments suggest that pheromonal signals processed through these systems have the potential to activate these neurons (Coquelin et al., 1984; Meredith and Fewell, 2001; Pfeiffer and Johnston, 1994; Westberry and Meredith, 2003a,b).”
BackgroundMoeller, J. F., & Meredith, M. J. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00683-0 · Cited by 17 · see citing works
The Role of the Vomeronasal Organ in Behavioral Control of Reproduction
JOHNS, M. A. (1986) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1986.tb28007.x · Cited by 16 · see citing works
Dudley, C. A., Chakravarty, S., & Barnea, A. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02820-7 · Cited by 15 · see citing works
Wirsig‐Wiechmann, C. R. (1993) · Physiology & Behavior · doi:10.1016/0031-9384(93)90201-p · Cited by 15 · see citing works
Anand, S., Turek, F. W., & Horton, T. H. (2004) · Biology of Reproduction · doi:10.1095/biolreprod.103.019380 · Cited by 14 · see citing works
“This is in contrast with the well-documented ability of urine from female mice to induce LH and testosterone secretion in male mice [5, 6, 9, 30, 31].”
ResultSelective enhancement of main olfactory input to the medial amygdala by GnRH
Blake, C. B., & Meredith, M. J. (2009) · Brain Research · doi:10.1016/j.brainres.2009.10.078 · Cited by 13 · see citing works
“Inmalemice, the LH increase occurs within 5 min of female chemosensory exposure (Coquelin et al., 1984), implying a rapid intracerebral release of GnRH.”
BackgroundInfluentialAlmeida, R. G., Flório, J. C., Spinosa, H. D. S., & Bernardi, M. M. (2002) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(02)00203-9 · Cited by 11 · see citing works
- Authors
- Coquelin, A., Clancy, A., Macrides, F., Noble, E., & Gorski, R.
- Affiliations
- University of California, Los Angeles (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1984-09-01
- Volume
- 4
- Issue
- 9
- Pages
- 2230-2236
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6564801
- OpenAlex
- W1868854124
- Cited by
- 127
- References
- 24
- Citations by year
- 2022: 1 · 2021: 1 · 2018: 2 · 2016: 1 · 2015: 3 · 2014: 4 · 2013: 3 · 2012: 3
- FWCI
- 4.34
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (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, vomeronasal system, luteinizing hormone, pheromones, chemosensory communication, male mice, female urine, ovariectomized females, reproductive hormones, intraspecific communication
- MeSH terms
- Animals, Castration, Horseradish Peroxidase, Luteinizing Hormone, Male, Mice, Inbred Strains, Nose, Pheromones, Sex Attractants, Mice
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