Impaired discrimination of and aversion to parasitized male odors by female oxytocin knockout mice
Abstract
A major cost of social behavior is the increased risk of exposure to parasites, with animals utilizing social information to recognize and avoid infected conspecifics. In mice, females can discriminate between infected and uninfected males on the basis of social cues, displaying aversive responses to the odors of infected males. In the present study, using female mice whose gene for oxytocin (OT) has been selectively deleted (OT knockout mice (OTKO)), we show that at least one normal allele for OT is required for the mediation of the recognition and avoidance of parasitized males. Female wild type (OTWT) and heterozygous (OTHZ) mice distinguished between the odors of individual males infected with the louse, Polyplax serrata, and uninfected males while the KO mice did not. Exposure to the odors of infected males induced analgesia in OTWT and OTHZ females, with OTKO females displaying attenuated analgesia. OTWT and OTHZ females, but not the OTKO females, also distinguished between the odors of novel and familiar infected males and modulated their analgesic responses on the basis of prior familiarity. In an odor choice test, OTWT and OTHZ females displayed a marked initial choice for the odors of uninfected males, whereas the OTKO females showed no consistent choice. This impairment was specific to the odors of infected males. OTKO females displayed normal analgesic responses to another aversive social odor, that of a stressed male, and an aversive non-social odor, that of a cat. The OTKOs had normal non-social olfactory memory, but were impaired in their social odor memory. These findings indicate that a normal OT gene comprises an essential part of the central recognition mechanism whereby females can both reduce the transmission of parasites to themselves and select for parasite-free males.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
OT has been shown to be important for social recognition memory.
“OT has been shown to be important for this memory ability (for a detailed review see Choleris in this issue [67]).”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [67]
Cites
1 retracted
Lund, I., Yu, L., Uvnas‐Moberg, K., Wang, J., Yu, C., Kurosawa, M., Agren, G., Rosén, A., Lekman, M., & Lundeberg, T. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02087.x · Cited by 181 · see citing works
RetractedHeritable True Fitness and Bright Birds: A Role for Parasites?
Hamilton, W. D., & Zuk, M. (1982) · Science · doi:10.1126/science.7123238 · Cited by 3,733 · see citing works
The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089 · see citing works
VARIATION IN MATE CHOICE AND MATING PREFERENCES: A REVIEW OF CAUSES AND CONSEQUENCES
Jennions, M. D., & Petrie, M. (1997) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1017/s0006323196005014 · Cited by 1,297 · see citing works
Social amnesia in mice lacking the oxytocin gene
Ferguson, J. N., Young, L. J., Hearn, E. F., Matzuk, M. M., Insel, T. R., & Winslow, J. T. (2000) · Nature Genetics · doi:10.1038/77040 · Cited by 1,130 · see citing works
Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08278.2001 · Cited by 1,043 · see citing works
Female sticklebacks use male coloration in mate choice and hence avoid parasitized males
Milinski, M., & Bakker, T. C. M. (1990) · Nature · doi:10.1038/344330a0 · Cited by 861 · see citing works
Control of mating preferences in mice by genes in the major histocompatibility complex.
Yamazaki, K., Boyse, E. A., Miké, V., Thaler, H. T., Mathieson, B. J., Abbott, J., Boyse, J., Zayas, Z. A., & Thomas, L. (1976) · The Journal of Experimental Medicine · doi:10.1084/jem.144.5.1324 · Cited by 687 · see citing works
Individual recognition in mice mediated by major urinary proteins
Hurst, J. L., Payne, C. E., Nevison, C. M., Marie, A. D., Humphries, R. E., Robertson, D. H. L., Cavaggioni, A., & Beynon, R. J. (2001) · Nature · doi:10.1038/414631a · Cited by 605 · see citing works
Social Barriers to Pathogen Transmission in Wild Animal Populations
Loehle, C. (1995) · Ecology · doi:10.2307/1941192 · Cited by 517 · see citing works
The neuroendocrine basis of social recognition
Ferguson, J. N., Young, L. J., & Insel, T. R. (2002) · Frontiers in Neuroendocrinology · doi:10.1006/frne.2002.0229 · Cited by 494 · see citing works
Dhabhar, F. S. (2002) · Brain Behavior and Immunity · doi:10.1016/s0889-1591(02)00036-3 · Cited by 464 · see citing works
Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic
Blanchard, D. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00009-4 · Cited by 461 · see citing works
VARIATION IN MATE CHOICE AND MATING PREFERENCES: A REVIEW OF CAUSES AND CONSEQUENCES
Jennions, M. D., & Petrie, M. (1997) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.1997.tb00015.x · Cited by 459 · see citing works
Neumann, Wigger, Torner, Holsboer, & Landgraf (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00442.x · Cited by 452 · see citing works
Measuring female mating preferences
Wagner, W. E. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0635 · Cited by 448 · see citing works
Bale, T. L., Davis, A. M., Auger, A. P., Dorsa, D. M., & McCarthy, M. M. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-07-02546.2001 · Cited by 446 · see citing works
Pathogens and the Evolution of Primate Sociality
Freeland, W. J. (1976) · Biotropica · doi:10.2307/2387816 · Cited by 437 · see citing works
Chemical signals and parasite-mediated sexual selection
Penn, D. J. (1998) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(98)01473-6 · Cited by 401 · see citing works
Barnard, C. J. (1990) · CRC Press eBooks · doi:10.1201/b12650 · Cited by 390 · see citing works
Choleris, E., Gustafsson, J.-Å., Korach, K. S., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0631699100 · Cited by 386 · see citing works
Self-citationInfant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse
Winslow, J. T., Hearn, E. F., Ferguson, J., Young, L. J., Matzuk, M. M., & Insel, T. R. (2000) · Hormones and Behavior · doi:10.1006/hbeh.1999.1566 · Cited by 348 · see citing works
Urine marking in populations of wild house mice Mus domesticus rutty. I. Communication between males
Hurst, J. L. (1990) · Animal Behaviour · doi:10.1016/s0003-3472(05)80916-9 · Cited by 335 · see citing works
An Anxiolytic Action of Oxytocin is Enhanced by Estrogen in the Mouse
MCCARTHY, M. M., MCDONALD, C. H., BROOKS, P. J., & GOLDMAN, D. (1996) · Physiology & Behavior · doi:10.1016/s0031-9384(96)00212-0 · Cited by 328 · see citing works
Ectoparasites: Direct impact on host fitness
Lehmann, T. (1993) · Parasitology Today · doi:10.1016/0169-4758(93)90153-7 · Cited by 327 · see citing works
Neumann, I. D., Krömer, S. A., Toschi, N., & Ebner, K. (2000) · Regulatory Peptides · doi:10.1016/s0167-0115(00)00197-x · Cited by 285 · see citing works
Volatile signals of the major histocompatibility complex in male mouse urine
Singer, A. G., Beauchamp, G. K., & Yamazaki, K. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.6.2210 · Cited by 248 · see citing works
Opposing actions of prostaglandins and oxytocin determine the onset of murine labor
Gross, G. A., Imamura, T., Luedke, C., Vogt, S. K., Olson, L. M., Nelson, D. M., Sadovsky, Y., & Muglia, L. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11875 · Cited by 238 · see citing works
Self-citationMate Choice in Experimentally Parasitized Rock Doves: Lousy Males Lose
Clayton, D. H. (1990) · American Zoologist · doi:10.1093/icb/30.2.251 · Cited by 221 · see citing works
The major histocompatibility complex and female mating preferences in mice
Egid, K., & Brown, J. L. (1989) · Animal Behaviour · doi:10.1016/s0003-3472(89)80051-x · Cited by 206 · see citing works
Social and individual recognition in rodents: Methodological aspects and neurobiological bases
Gheusi, G., Bluthé, R.-M., Goodall, G., & Dantzer, R. (1994) · Behavioural Processes · doi:10.1016/0376-6357(94)90060-4 · Cited by 206 · see citing works
Discrimination by female mice between the odours of parasitized and non-parasitized males
Kavaliers, M., & Colwell, D. D. (1995) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1995.0113 · Cited by 205 · see citing works
Self-citationParasites and the Coexistence of Animal Host Species
Freeland, W. J. (1983) · The American Naturalist · doi:10.1086/284052 · Cited by 191 · see citing works
Parasite load predicts mate choice in guppies
KENNEDY, C. E. J., Endler, J. A., Poynton, S. L., & McMinn, H. (1987) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00299966 · Cited by 190 · see citing works
Parasites and the Evolution of Host Social Behavior
Møller, A., Dufva, R., & Allander, K. (1993) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60405-2 · Cited by 189 · see citing works
The Role of Parasites in Sexual Selection: Current Evidence and Future Directions
Zuk, M. (1992) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60141-2 · Cited by 188 · see citing works
Multiple roles of major urinary proteins in the house mouse, Mus domesticus
Beynon, R. J., & Hurst, J. L. (2003) · Biochemical Society Transactions · doi:10.1042/bst0310142 · Cited by 173 · see citing works
Detailed information about parasites revealed by sexual ornamentation
Wedekind, C. (1992) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1992.0024 · Cited by 170 · see citing works
Windle, R. J., Shanks, N., Lightman, S. L., & Ingram, C. D. (1997) · Endocrinology · doi:10.1210/en.138.7.2829 · Cited by 170 · see citing works
Dluzen, D. E., Muraoka, S., Engelmann, M., & Landgraf, R. (1998) · Peptides · doi:10.1016/s0196-9781(98)00047-3 · Cited by 169 · see citing works
Cue and context conditioning of defensive behaviors to cat odor stimuli
Blanchard, R. J., Yang, M., Li, C.-I., Gervacio, A., & Blanchard, D. C. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00043-4 · Cited by 168 · see citing works
The contagion indicator hypothesis for parasite-mediated sexual selection.
Able, D. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.5.2229 · Cited by 167 · see citing works
Exposure to a cat produces opioid analgesia in rats.
Lester, L. S., & Fanselow, M. S. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.4.756 · Cited by 161 · see citing works
Exposure to a cat produces opioid analgesia in rats.
Lester, L. S., & Fanselow, M. S. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.4.756 · Cited by 160 · see citing works
Endogenous oxytocin is involved in short-term olfactory memory in female rats
Engelmann, M., Ebner, K., Wotjak, C. T., & Landgraf, R. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00084-3 · Cited by 156 · see citing works
Odors released by stressed rats produce opioid analgesia in unstressed rats.
Fanselow, M. S. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.3.589 · Cited by 152 · see citing works
Oxytocin mediates stress‐induced analgesia in adult mice
Robinson, D. A., Wei, F., Wang, G. D., Li, P., Kim, S. J., Vogt, S. K., Muglia, L. J., & Zhuo, M. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013492 · Cited by 148 · see citing works
Self-citationHost resistance in cattle tick control
de Castro, J. J., & Newson, R. M. (1993) · Parasitology Today · doi:10.1016/0169-4758(93)90154-8 · Cited by 147 · see citing works
Potts, W. K., Manning, C. J., & Wakeland, E. K. (1994) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1994.0154 · Cited by 142 · see citing works
Odors released by stressed rats produce opioid analgesia in unstressed rats.
Fanselow, M. S. (1985) · Behavioral Neuroscience · doi:10.1037/0735-7044.99.3.589 · Cited by 138 · see citing works
Hurst, J. L. (1990) · Animal Behaviour · doi:10.1016/s0003-3472(05)80918-2 · Cited by 136 · see citing works
Odours of parasitized males induce aversive responses in female mice
Kavaliers, M., & Colwell, D. D. (1995) · Animal Behaviour · doi:10.1016/0003-3472(95)80032-8 · Cited by 131 · see citing works
Self-citationChewing and sucking lice as parasites of mammals and birds
Price, M. A., & Graham, O. H. (1997) · Cited by 123 · see citing works
Kose, M., Mänd, R., & Møller, A. P. (1999) · Animal Behaviour · doi:10.1006/anbe.1999.1249 · Cited by 120 · see citing works
Behavioral Adaptations to Parasites: An Ethological Approach
Hart, B. L. (1992) · Journal of Parasitology · doi:10.2307/3283472 · Cited by 113 · see citing works
Social behavior and comparative genomics: new genes or new gene regulation?
Robinson, G. E., & Ben‐Shahar, Y. (2002) · Genes Brain & Behavior · doi:10.1034/j.1601-183x.2002.10401.x · Cited by 101 · see citing works
Sex differences in opioid and non-opioid mediated predator-induced analgesia in mice
Kavaliers, M., & Colwell, D. D. (1991) · Brain Research · doi:10.1016/0006-8993(91)91394-g · Cited by 98 · see citing works
Self-citationInfluenza Infection Neutralizes the Attractiveness of Male Odour to Female Mice (Mus musculus)
Penn, D. J., Schneider, G., White, K., Slev, P. R., & Potts, W. K. (1998) · Ethology · doi:10.1111/j.1439-0310.1998.tb00102.x · Cited by 95 · see citing works
Kavaliers, M., Fudge, M. A., Colwell, D. D., & Choleris, E. (2003) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-003-0631-2 · Cited by 92 · see citing works
Self-citationThe consequences of inbreeding for recognizing competitors
Nevison, C. M., Barnard, C. J., Beynon, R. J., & Hurst, J. L. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1057 · Cited by 86 · see citing works
Kavaliers, M., Colwell, D. D., Braun, W. J., & Choleris, E. (2003) · Animal Behaviour · doi:10.1006/anbe.2002.2043 · Cited by 82 · see citing works
Self-citationPedersen, C. A., & Boccia, M. L. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2001.1736 · Cited by 81 · see citing works
Ehman, K. D., & Scott, M. E. (2001) · Animal Behaviour · doi:10.1006/anbe.2001.1805 · Cited by 79 · see citing works
Nomura, M., Saito, J., Ueta, Y., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01095.x · Cited by 69 · see citing works
Self-citationChemosensation and genetic individuality
Singh, P. B. (2001) · Reproduction · doi:10.1530/rep.0.1210529 · Cited by 68 · see citing works
What is the role of the immune system in determining individually distinct body odours?
Brown, R. E. (1995) · International Journal of Immunopharmacology · doi:10.1016/0192-0561(95)00052-4 · Cited by 65 · see citing works
Mate Choice for Non‐siblings in Wild House Mice: Evidence from a Choice Test and a Reproductive Test
Krackow, S., & Matuschak, B. (1991) · Ethology · doi:10.1111/j.1439-0310.1991.tb00266.x · Cited by 63 · see citing works
Kavaliers, M., Colwell, D. D., Ossenkopp, K., & Perrot-Sinal, T. S. (1997) · Behavioral Ecology and Sociobiology · doi:10.1007/s002650050353 · Cited by 56 · see citing works
Self-citationThe ecology of the louse Polyplax serrataq (Burn.) on the Mouse Mus musculus L.
Murray, M. (1961) · Australian Journal of Zoology · doi:10.1071/zo9610001 · Cited by 55 · see citing works
Influence of host behaviour on some ectoparasites of birds and mammals
Murray, M. D., Barnard, C. J., & Behnke, J. M. (1990) · Cited by 49 · see citing works
Kavaliers, M., Colwell, D. D., & Choleris, E. (2000) · Parasitology Today · doi:10.1016/s0169-4758(00)01786-5 · Cited by 44 · see citing works
Self-citationParasitic infection impairs spatial learning in mice
Kavaliers, M., Colwell, D. D., & Galea, L. A. M. (1995) · Animal Behaviour · doi:10.1006/anbe.1995.0234 · Cited by 41 · see citing works
Self-citationMurine Immune Responses and Immunization Against Polyplax serrata (Anoplura: Polyplacidae)
Ratzlaff, R. E., & Wikel, S. K. (1990) · Journal of Medical Entomology · doi:10.1093/jmedent/27.6.1002 · Cited by 22 · see citing works
Exposure to mosquitoes, Aedes togoi (Theo.), induces and augments opioid-mediated analgesia in mice
Colwell, D. D., & Kavaliers, M. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90334-z · Cited by 16 · see citing works
Self-citationNew genomic avenues in behavioural neuroendocrinology *
Lightman, S. L., Insel, T. R., & Ingram, C. D. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02082.x · Cited by 13 · see citing works
Nelson, W. A., Bell, J. F., & Stewart, S. J. (1979) · Experimental Parasitology · doi:10.1016/0014-4894(79)90107-3 · Cited by 13 · see citing works
Effects of limb disability on lousiness of mice
Lodmell, D. L., Bell, J. F., Clifford, C. M., Moore, G. J., & Raymond, G. H. (1970) · Experimental Parasitology · doi:10.1016/0014-4894(70)90024-x · Cited by 11 · see citing works
Nelson, W. A., Bell, J. F., Stewart, S., & Kozub, G. C. (1983) · Journal of Medical Entomology · doi:10.1093/jmedent/20.5.551 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior
Ross, H. E., & Young, L. J. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.004 · Cited by 856 · see citing works
“OTKO female mice also are unable to discriminate parasite load on potential mates, which would increase their risk of infection [79].”
BackgroundBrain oxytocin: A key regulator of emotional and social behaviours in both females and males
Neumann, I. D. (2008) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2008.01726.x · Cited by 743 · see citing works
Oxytocin, vasopressin, and social recognition in mammals
Bielsky, I. F., & Young, L. J. (2004) · Peptides · doi:10.1016/j.peptides.2004.05.019 · Cited by 460 · see citing works
Ross, H. E., Freeman, S. M., Spiegel, L. L., Ren, X., Terwilliger, E. F., & Young, L. J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5039-08.2009 · Cited by 322 · see citing works
Crawley, J. N., Chen, T., Puri, A., Washburn, R., Sullivan, T. L., Hill, J. M., Young, N. B., Nadler, J. J., Moy, S. S., Young, L. J., et al. (2007) · Neuropeptides · doi:10.1016/j.npep.2007.02.002 · Cited by 232 · see citing works
Genes, hormones, and circuits: An integrative approach to study the evolution of social behavior
O’Connell, L. A., & Hofmann, H. A. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.12.004 · Cited by 227 · see citing works
Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition
Gabor, C. S., Phan, A., Clipperton-Allen, A. E., Kavaliers, M., & Choleris, E. (2012) · Behavioral Neuroscience · doi:10.1037/a0026464 · Cited by 221 · see citing works
Self-citationNeuroendocrinology of social information processing in rats and mice
Choleris, E., Clipperton-Allen, A. E., Phan, A., & Kavaliers, M. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.003 · Cited by 205 · see citing works
Self-citationOxytocin role in enhancing well-being: A literature review
IsHak, W. W., Kahloon, M., & Fakhry, H. (2010) · Journal of Affective Disorders · doi:10.1016/j.jad.2010.06.001 · Cited by 198 · see citing works
Choleris, E., Ogawa, S., Kavaliers, M., Gustafsson, J.-Α., Korach, K. S., Muglia, L. J., & Pfaff, D. W. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00203.x · Cited by 173 · see citing works
Self-citationNeumann, I. D. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.04.012 · Cited by 162 · see citing works
Olfactory-mediated parasite recognition and avoidance: linking genes to behavior.
Kavaliers, M., Choleris, E., Ågmo, A., & Pfaff, D. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.03.005 · Cited by 128 · see citing works
Self-citationArakawa, H., Arakawa, K., & Terrence Deak, B. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.013 · Cited by 114 · see citing works
OxytocinSynthesis, Secretion, and Reproductive Functions
BURBACH, J., YOUNG, L., & RUSSELL, J. (2006) · Knobil and Neill's Physiology of Reproduction · doi:10.1016/b978-012515400-0/50063-4 · Cited by 113 · see citing works
Kavaliers, M., Choleris, E., & Pfaff, D. W. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.011 · Cited by 112 · see citing works
Self-citationGillespie, S. M., Mitchell, I., Fisher, D. D., & Beech, A. R. (2012) · Aggression and Violent Behavior · doi:10.1016/j.avb.2012.03.005 · Cited by 109 · see citing works
Kavaliers, M., Colwell, D. D., & Choleris, E. (2005) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-004-0896-0 · Cited by 102 · see citing works
Self-citationGenes, odours and the recognition of parasitized individuals by rodents.
Kavaliers, M., Choleris, E., & Pfaff, D. (2005) · Trends in Parasitology · doi:10.1016/j.pt.2005.07.008 · Cited by 101 · see citing works
Self-citationInadvertent social information and the avoidance of parasitized male mice: A role for oxytocin
Kavaliers, M., Choleris, E., Ågmo, A., Braun, W. J., Colwell, D. D., Muglia, L. J., Ogawa, S., & Pfaff, D. W. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600410103 · Cited by 87 · see citing works
Self-citationThe role of social cognition in parasite and pathogen avoidance
Kavaliers, M., & Choleris, E. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2017.0206 · Cited by 85 · see citing works
Self-citationCao, Y., Wu, R., Tai, F., Zhang, X., Yu, P., An, X., Qiao, X., & Hao, P. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.11.005 · Cited by 82 · see citing works
Oxytocin and the oxytocin receptor underlie intrastrain, but not interstrain, social recognition
Macbeth, A. H., Lee, H. ‐., Edds, J., & Young, W. S. (2009) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2009.00506.x · Cited by 81 · see citing works
Oxytocin and behavior: lessons from knockout mice
Caldwell, H. K., Aulino, E. A., Freeman, A. R., Miller, T. V., & Witchey, S. K. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22431 · Cited by 79 · see citing works
Estrogenic involvement in social learning, social recognition and pathogen avoidance
Choleris, E., Clipperton‐Allen, A. E., Phan, A., Valsecchi, P., & Kavaliers, M. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.02.001 · Cited by 77 · see citing works
Self-citationFunctional Genomics of Social Recognition
Choleris, E., Kavaliers, M., & Pfaff, D. W. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.0953-8194.2004.01178.x · Cited by 75 · see citing works
Self-citationHasshoff, M., Höhnisch, C., Tonn, D., Hasert, B., & Hinrich Schulenburg, Y. (2007) · The FASEB Journal · doi:10.1096/fj.06-6551com · Cited by 71 · see citing works
Parasite-augmented mate choice and reduction in innate fear in rats infected byToxoplasma gondii
Vyas, A. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.072983 · Cited by 69 · see citing works
Towards a neurobiological model of offending
Mitchell, I., & Beech, A. R. (2011) · Clinical Psychology Review · doi:10.1016/j.cpr.2011.04.001 · Cited by 65 · see citing works
Genetic Influences on Aggressive Behaviors and Arousability in Animals
Ogawa, S., Choleris, E., & Pfaff, D. W. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1330.016 · Cited by 59 · see citing works
Self-citationSocial neuroscience of disgust
Kavaliers, M., Ossenkopp, K., & Choleris, E. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12508 · Cited by 58 · see citing works
Self-citationRodent models for autism: A critical review
Belzung, C., Leman, S., Vourc’h, P., & Andres, C. R. (2005) · Drug Discovery Today Disease Models · doi:10.1016/j.ddmod.2005.05.004 · Cited by 43 · see citing works
Wang, L., Hou, W., He, Z., Yuan, W., Yang, J., Yang, Y., Jia, R., Zhu, Z., Zhou, Y., & Tai, F. (2017) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.11.002 · Cited by 43 · see citing works
Baker, D. G. (2007) · doi:10.1002/9780470344552.ch11 · Cited by 42 · see citing works
Clinical and Neurobiological Relevance of Current Animal Models of Autism Spectrum Disorders
Kim, K. C., Gonzales, E. L., Lázaro, M. T., Choi, C. S., Bahn, G. H., Yoo, H. J., & Shin, C. Y. (2016) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2016.061 · Cited by 40 · see citing works
Annual Research Review: Transgenic mouse models of childhood‐onset psychiatric disorders
Robertson, H. R., & Feng, G. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2011.02380.x · Cited by 33 · see citing works
Kavaliers, M., Ågmo, A., Choleris, E., Gustafsson, J.-Å., Korach, K. S., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2004) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2004.00068.x · Cited by 33 · see citing works
Self-citationInfection threat shapes our social instincts
Krämer, P., & Bressan, P. (2021) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-021-02975-9 · Cited by 30 · see citing works
Social factors and the neurobiology of pathogen avoidance
Kavaliers, M., Ossenkopp, K., Tyson, C.-D., Bishnoi, I. R., & Choleris, E. (2022) · Biology Letters · doi:10.1098/rsbl.2021.0371 · Cited by 28 · see citing works
Self-citationKavaliers, M., Choleris, E., Ågmo, A., Muglia, L. J., Ogawa, S., & Pfaff, D. W. (2005) · Animal Behaviour · doi:10.1016/j.anbehav.2004.12.016 · Cited by 28 · see citing works
Self-citationMooney, S. J., & Holmes, M. M. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.11.014 · Cited by 27 · see citing works
The Role of Estrogen Receptors in the Regulation of Aggressive Behaviors
Ogawa, S., Nomura, M. J., Choleris, E., & Pfaff, D. W. (2005) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195168761.003.0010 · Cited by 25 · see citing works
Self-citationArakawa, H. (2021) · Current Research in Neurobiology · doi:10.1016/j.crneur.2021.100011 · Cited by 24 · see citing works
Coria-Avila, G. A., Herrera-Covarrubias, D., García, L. I., Toledo, R., Hernández, M. E., Paredes-Ramos, P., Corona-Morales, A. A., & Manzo, J. (2022) · Animals · doi:10.3390/ani12243589 · Cited by 25 · see citing works
Becker, R. O., Lazzari, V. M., Menezes, I. C., Morris, M., Rigatto, K., Lucion, A. B., Rasia‐Filho, A. A., & Giovenardi, M. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.07.034 · Cited by 21 · see citing works
Zimmermann-Peruzatto, J. M., Lazzari, V. M., Agnes, G., Becker, R. O., de Moura, A. C., Guedes, R. P., Lucion, A. B., Almeida, S., & Giovenardi, M. (2016) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-016-0419-3 · Cited by 21 · see citing works
Sevoflurane impairs post-operative olfactory memory but preserves olfactory function
Kostopanagiotou, G. G., Kalimeris, K. A., Kesidis, K., Matsota, P. K., Dima, C., Economou, M., & Papageorgiou, C. (2010) · European Journal of Anaesthesiology · doi:10.1097/eja.0b013e328340702b · Cited by 21 · see citing works
Maternal Brain Adaptations in Pregnancy
Brunton, P. J., & Russell, J. A. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00044-2 · Cited by 18 · see citing works
The Role of the Oxytocin/Arginine Vasopressin System in Animal Models of Autism Spectrum Disorder
Zhang, R., Xu, X., Zhang, H.-F., Han, S., & Han, J. (2017) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-319-52498-6_8 · Cited by 16 · see citing works
Mechanisms underlying sexual and affiliative behaviors of mice: relation to generalized CNS arousal
Shelley, D. N., Choleris, E., Kavaliers, M., & Pfaff, D. W. (2006) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsl032 · Cited by 16 · see citing works
Self-citationSocial Cognition and Oxytocin in Huntington’s Disease: New Insights
Unti, E., Mazzucchi, S., Frosini, D., Pagni, C., Tognoni, G., Palego, L., Betti, L., Miraglia, F., Giannaccini, G., & Ceravolo, R. (2018) · Brain Sciences · doi:10.3390/brainsci8090161 · Cited by 15 · see citing works
Paletta, P., Bass, N., Kavaliers, M., & Choleris, E. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0058 · Cited by 15 · see citing works
Self-citationChronic central oxytocin infusion impairs sociability in mandarin voles
Du, P., He, Z., Cai, Z., Hao, X., Dong, N., Yuan, W., Hou, W., Yang, J., Jia, R., & Tai, F. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.09.006 · Cited by 14 · see citing works
The evolutionary origins of mating failures and multiple mating
Gowaty, P. A., & Hubbell, S. P. (2012) · Entomologia Experimentalis et Applicata · doi:10.1111/eea.12023 · Cited by 13 · see citing works
Odor Cues Released by Ehrlich Tumor-Bearing Mice Are Aversive and Induce Psychological Stress
Alves, G. J., & Palermo‐Neto, J. (2014) · NeuroImmunoModulation · doi:10.1159/000358253 · Cited by 13 · see citing works
Mate Selection, Sexual Orientation, and Pair Bonding
Balthazart, J., & Young, L. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00048-x · Cited by 12 · see citing works
Sobrian, S., & Holson, R. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00066 · Cited by 14 · see citing works
The Neurobiology and Genetics of Affiliation and Social Bonding in Animal Models
Donaldson, Z. R., & Young, L. J. (2016) · Springer eBooks · doi:10.1007/978-1-4939-3777-6_4 · Cited by 11 · see citing works
Prosocial effects of prolactin in male rats: Social recognition, social approach and social learning
Donhoffner, M. E., Saleh, S. A., Schink, O., & Wood, R. I. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.09.011 · Cited by 10 · see citing works
Hormonal and Pheromonal Modulation of the Extended Amygdala: Implications for Social Behavior
Swann, J. M., Fabre‐Nys, C., & Barton, R. A. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00012-7 · Cited by 10 · see citing works
Neumann, I. D. (2008) · Springer eBooks · doi:10.1007/978-3-540-79288-8_7 · Cited by 8 · see citing works
Pillay, N., & Rymer, T. L. (2010) · Behaviour · doi:10.1163/000579510x505445 · Cited by 8 · see citing works
Kim, C.-K., Sakudo, A., Taniuchi, Y., Shigematsu, K., Kang, C.-B., Saeki, K., Matsumoto, Y., Sakaguchi, S., Itohara, S., & Onodera, T. (2007) · International Journal of Molecular Medicine · doi:10.3892/ijmm.20.2.169 · Cited by 7 · see citing works
The involvement of oxytocin and vasopressin in social recognition and social learning
Dore, R., Phan, A., Clipperton‐Allen, A. E., Kavaliers, M., & Choleris, E. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.016 · Cited by 7 · see citing works
Self-citationStud male-originating chemosignals: a luteotrophic agent.
Archunan, G. (2014) · PubMed · Cited by 7 · see citing works
Pathogen and Toxin Disgust in Rodents
Kavaliers, M., Ossenkopp, K., & Choleris, E. (2021) · Springer eBooks · doi:10.1007/978-3-030-84486-8_4 · Cited by 5 · see citing works
Self-citationJohnson, C. E., Hammock, E. A. D., & Dewan, A. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105302 · Cited by 5 · see citing works
Olfaction-Mediated Pathogen Avoidance in Mammals
Schwambergová, D., Fialová, J., & Havlı́ček, J. (2023) · Springer eBooks · doi:10.1007/978-3-031-35159-4_12 · Cited by 4 · see citing works
Neuroendocrinology, Neurochemistry, and Molecular Neurobiology of Affiliative Behavior
Hammock, E. A. D., & Young, L. J. (2006) · Springer eBooks · doi:10.1007/978-0-387-30405-2_6 · Cited by 4 · see citing works
Genetic Transmission of Behavior and Its Neuroendocrine Correlates
Hambsch, B., Landgraf, R., Czibere, L., & Touma, C. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00084-x · Cited by 2 · see citing works
Oxytocin, vasopressin, sociality, and pathogen avoidance
Kavaliers, M., & Choleris, E. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.017 · Cited by 1 · see citing works
Self-citationYoung, W. S. (2013) · Endocrinology · doi:10.1210/en.2013-1885 · Cited by 1 · see citing works
Choleris, E., Pfaff, D. W., & Kavaliers, M. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.021 · Cited by 1 · see citing works
Self-citationThe Oxytocin System: Single Gene Effects on Social Behavior Across Species
Temple, J. A., & Donaldson, Z. R. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.90056-6 · Cited by 1 · see citing works
Young, L. J., & Zingg, H. H. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00056-0
Sassano, M. F. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/wwr3-7m34
GBAKER, D. (2007) · Elsevier eBooks · doi:10.1016/b978-012369454-6/50051-0
Young, L. J., & Zingg, H. H. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00048-6
Crawley, J. N. (2006) · Wiley eBooks · doi:10.1002/9780470119051.refs
- Authors
- Kavaliers, M., Colwell, D. D., Choleris, E., Ågmo, A., Muglia, L. J., Ogawa, S., & Pfaff, D. W.
- Affiliations
- Western University (CA)
- Agriculture and Agri-Food Canada (CA)
- University of Guelph (CA)
- UiT The Arctic University of Norway (NO)
- Washington University in St. Louis (US)
- Rockefeller University (US)
- Venue
- Genes, Brain and Behavior
- Publisher
- Wiley
- Published
- 2003-08
- Volume
- 2
- Issue
- 4
- Pages
- 220-230
- ISSN
- 1601-183X (ISSN-L)
- 1601-1848
- OpenAlex
- W2002790995
- Cited by
- 78
- References
- 77
- Citations by year
- 2023: 2 · 2022: 3 · 2021: 3 · 2019: 1 · 2018: 4 · 2017: 4 · 2016: 5 · 2014: 4 · 2013: 6 · 2012: 5
- FWCI
- 7.89
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Genes Brain & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada
- Agriculture and Agri-Food Canada
- National Institute of Mental Health (MH 38273, R01MH038273, MH-62147, R01MH062147)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- oxytocin, parasite avoidance, analgesia, heterozygous females, female mate choice, social information use
- MeSH terms
- Animals, Anoplura, Behavior, Animal, Discrimination, Psychological, Female, Male, Odorants, Orchiectomy, Oxytocin, Social Behavior, Species Specificity, Stress, Psychological, Mice, Knockout, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review