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Genomic Imprinting and Sexual Experience-Dependent Learning in the Mouse

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Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 2))

Abstract

Sexual experience is a significant modulator of behaviour in male rodents, inducing mating behaviour changes, increased sexual motivation and olfactory learning. Sexually experienced males exhibit greater motivation to investigate females and show preferences for receptive oestrous females and their odours which are not seen in virgins. These behavioural effects of sexual experience are accompanied by neurobiological changes affecting forebrain sensitivity to steroid hormones, mesolimbic dopamine function and neural activity in the basal hypothalamus and olfactory pathways. These changes suggest that sexually experienced males are better able to detect receptive females, are more motivated to pursue them and are more proficient copulators. Furthermore, this response to sexual experience appears to be mediated by imprinted genes. Imprinted genes are a small class of mammalian autosomal genes that are expressed in parent-of-origin fashion and which are key regulators of placentation and development in mammals. Mice carrying a knockout of the paternally expressed gene Peg3 have deficits in maternal care and offspring development, but Peg3 mutant males also fail to show any sexual experience-dependent changes in behaviour or learned olfactory preferences. There are also no changes in female odour-evoked neural activity in the hypothalamus, vomeronasal system or main olfactory pathway of Peg3 mutants after sexual experience, suggesting a deficit in sexual experience-dependent forebrain plasticity. Peg3 appears to regulate male behavioural traits that would enhance its own transmission down the male line, suggesting that this imprinted gene has evolved to directly influence plasticity in male reproductive behaviour.

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References

  • Allen, N. D., Logan, K., Lally, G., Drage, D. J., Norris, M. L., & Keverne, E. B. (1995). Distribution of parthenogenetic cells in the mouse brain and their influence on brain development and behavior. Proceedings of the National Academy of Sciences of the United States of America, 92, 10782–10786.

    Article  PubMed  CAS  Google Scholar 

  • Arletti, R., Bazzani, C., Castelli, M., & Bertolini, A. (1985). Oxytocin improves male copulatory performance in rats. Hormones and Behavior, 19, 14–20.

    Article  PubMed  CAS  Google Scholar 

  • Balfour, M. E., Yu, L., & Coolen, L. M. (2004). Sexual behavior and sex-associated environmental cues activate the mesolimbic system in male rats. Neuropsychopharmacology, 29, 718–730.

    Article  PubMed  CAS  Google Scholar 

  • Barlow, D. (1993). Methylation and imprinting: From host defense to gene regulation? Science, 260, 309–310.

    Article  PubMed  CAS  Google Scholar 

  • Barr, G. A. (1981). Effects of different housing conditions on intraspecies fighting between male Long-Evans hooded rats. Physiology & Behavior, 27, 1041–1044.

    Article  CAS  Google Scholar 

  • Barton, S. C., Ferguson-Smith, A. C., Fundele, R., & Surani, M. A. (1991). Influence of paternally imprinted genes on development. Development, 113, 679–687.

    PubMed  CAS  Google Scholar 

  • Barton, S. C., Surani, M. A., & Norris, M. L. (1984). Role of paternal and maternal genomes in mouse development. Nature, 311, 374–376.

    Article  PubMed  CAS  Google Scholar 

  • Baum, M. J., & Everitt, B. J. (1992). Increased expression of c-Fos in the medial preoptic area after mating in male rats: Role of afferent inputs from the medial amygdala and midbrain central tegmental field. Neuroscience, 50, 627–646.

    Article  PubMed  CAS  Google Scholar 

  • Beach, F. A. (1942). Comparison of copulatory behavior of male rats raised in isolation, cohabitation, and segregation. The Pedagogical Seminary and Journal of Genetic Psychology, 60, 121–136.

    Article  Google Scholar 

  • Brennan, P., & Kendrick, K. (2006). Mammalian social odours: Attraction and individual recognition. Philosophical Transactions of the Royal Society of London. Series B, 361, 2061–2078.

    Article  PubMed  CAS  Google Scholar 

  • Brennan, P. A., & Keverne, E. B. (1997). Neural mechanisms of mammalian olfactory learning. Progress in Neurobiology, 51, 457–481.

    Article  PubMed  CAS  Google Scholar 

  • Brennan, P. A., & Zufall, F. (2006). Pheromonal communication in vertebrates. Nature, 444, 308–315.

    Article  PubMed  CAS  Google Scholar 

  • Broad, K. D., Curley, J. P., & Keverne, E. B. (2009). Increased apoptosis during neonatal brain development underlies the adult behavioral deficits seen in mice lacking a functional paternally expressed gene 3 (Peg3). Developmental Neurobiology, 69, 314–325.

    Article  PubMed  CAS  Google Scholar 

  • Buck, L. B. (2000). The molecular architecture of odor and pheromone sensing in mammals. Cell, 100, 611–618.

    Article  PubMed  CAS  Google Scholar 

  • Burns-Cusato, M., Scordalakes, E. M., & Rissman, E. F. (2004). Of mice and missing data: What we know (and need to learn) about male sexual behavior. Physiology & Behavior, 83, 217–232.

    Article  CAS  Google Scholar 

  • Cameron, N. M., Champagne, F. A., Parent, C., Fish, E. W., Ozaki-Kuroda, K., & Meaney, M. J. (2005). The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neuroscience and Biobehavioral Reviews, 29, 843–865.

    Article  PubMed  Google Scholar 

  • Carr, W. J., Loeb, L. S., & Dissinger, M. L. (1965). Responses of rats to sex odors. Journal of Comparative and Physiological Psychology, 59, 370–377.

    Article  PubMed  CAS  Google Scholar 

  • Champagne, F. A., Curley, J. P., Swaney, W. T., Hasen, N. S., & Keverne, E. B. (2009). Paternal influence on female behavior: The role of Peg3 in exploration, olfaction and neuroendocrine regulation of maternal behavior of female mice. Behavioral Neuroscience, 123, 469–480.

    Article  PubMed  Google Scholar 

  • Chapman, D. D., Shivji, M. S., Louis, E., Sommer, J., Fletcher, H., & Prodohl, P. A. (2007). Virgin birth in a hammerhead shark. Biology Letters, 3, 425–427.

    Article  PubMed  Google Scholar 

  • Coan, P. M., Burton, G. J., & Ferguson-Smith, A. C. (2005). Imprinted genes in the placenta – a review. Placenta, 26(suppl A), S10–S20.

    Article  PubMed  CAS  Google Scholar 

  • Costantini, R. M., Park, J. H., Beery, A. K., Paul, M. J., Ko, J. J., & Zucker, I. (2007). Post-castration retention of reproductive behavior and olfactory preferences in male Siberian hamsters: Role of prior experience. Hormones and Behavior, 51, 149–155.

    Article  PubMed  Google Scholar 

  • Cuellar, O. (1976). Intraclonal histocompatibility in a parthenogenetic lizard: Evidence of genetic homogeneity. Science, 193, 150–153.

    Article  PubMed  CAS  Google Scholar 

  • Curley, J. P., Barton, S., Surani, A., & Keverne, E. B. (2004). Coadaptation in mother and infant regulated by a paternally expressed imprinted gene. Proceedings of the Royal Society of London. Series B, 271, 1303–1309.

    Article  PubMed  Google Scholar 

  • Damsma, G., Pfaus, J. G., Wenkstern, D., Phillips, A. G., & Fibiger, H. C. (1992). Sexual behavior increases dopamine transmission in the nucleus accumbens and striatum of male rats: Comparison with novelty and locomotion. Behavioral Neuroscience, 106, 181–191.

    Article  PubMed  CAS  Google Scholar 

  • Davies, W., Isles, A. R., Humby, T., & Wilkinson, L. S. (2008). What are imprinted genes doing in the brain? Advances in Experimental Medicine and Biology, 626, 62–70.

    Article  PubMed  CAS  Google Scholar 

  • Davies, W., Isles, A., Smith, R., Karunadasa, D., Burrmann, D., Humby, T., et al. (2005). Xlr3b is a new imprinted candidate for X-linked parent-of-origin effects on cognitive function in mice. Nature Genetics, 37, 625–629.

    Article  PubMed  CAS  Google Scholar 

  • Davies, W., Isles, A. R., & Wilkinson, L. S. (2001). Imprinted genes and mental dysfunction. Annali Medici, 33, 428–436.

    Article  CAS  Google Scholar 

  • DeChiara, T. M., Robertson, E. J., & Efstratiadis, A. (1991). Parental imprinting of the mouse insulin-like growth factor II gene. Cell, 64, 849.

    Article  PubMed  CAS  Google Scholar 

  • Deng, Y. B., & Wu, X. W. (2000). Peg3/Pw1 promotes p53-mediated apoptosis by inducing Bax translocation from cytosol to mitochondria. Proceedings of the National Academy of Sciences of the United States of America, 97, 12050–12055.

    Article  PubMed  CAS  Google Scholar 

  • Dewsbury, D. A. (1969). Copulatory behaviour of rats (Rattus norvegicus) as a function of prior copulatory experience. Animal Behaviour, 17, 217–223.

    Article  PubMed  CAS  Google Scholar 

  • Dominguez, J. M., Brann, J. H., Gil, M., & Hull, E. M. (2006). Sexual experience increases nitric oxide synthase in the medial preoptic area of male rats. Behavioral Neuroscience, 120, 1389–1394.

    Article  PubMed  CAS  Google Scholar 

  • Dominguez, J. M., & Hull, E. M. (2001). Stimulation of the medial amygdala enhances medial preoptic dopamine release: Implications for male rat sexual behavior. Brain Research, 917, 225–229.

    Article  PubMed  CAS  Google Scholar 

  • Dominguez, J. M., & Hull, E. M. (2005). Dopamine, the medial preoptic area, and male sexual behavior. Physiology & Behavior, 86, 356–368.

    Article  CAS  Google Scholar 

  • Dominguez, J., Riolo, J. V., Xu, Z., & Hull, E. M. (2001). Regulation by the medial amygdala of copulation and medial preoptic dopamine release. The Journal of Neuroscience, 21, 349–355.

    PubMed  CAS  Google Scholar 

  • Dorries, A., Spohr, H. L., & Kunze, J. (1988). Angelman (“happy puppet”) syndrome – seven new cases documented by cerebral computed tomography: Review of the literature. European Journal of Pediatrics, 148, 270–273.

    Article  PubMed  CAS  Google Scholar 

  • Edinger, K. L., & Frye, C. A. (2007). Sexual experience of male rats influences anxiety-like behavior and androgen levels. Physiology & Behavior, 92, 443–453.

    Article  CAS  Google Scholar 

  • Edwards, C. A., & Ferguson-Smith, A. C. (2007). Mechanisms regulating imprinted genes in clusters. Current Opinion in Cell Biology, 19, 281–289.

    Article  PubMed  CAS  Google Scholar 

  • Ferguson, J. N., Young, L. J., Hearn, E. F., Matzuk, M. M., Insel, T. R., & Winslow, J. T. (2000). Social amnesia in mice lacking the oxytocin gene. Nature Genetics, 25, 284–288.

    Article  PubMed  CAS  Google Scholar 

  • Fernandez-Guasti, A., Roldan-Roldan, G., & Saldivar, A. (1989). Reduction in anxiety after ejaculation in the rat. Behavioural Brain Research, 32, 23–29.

    Article  PubMed  CAS  Google Scholar 

  • Fewell, G. D., & Meredith, M. (2002). Experience facilitates vomeronasal and olfactory influence on Fos expression in medial preoptic area during pheromone exposure or mating in male hamsters. Brain Research, 941, 91–106.

    Article  PubMed  CAS  Google Scholar 

  • Flannelly, K. J., Blanchard, R. J., Muraoka, M. Y., & Flannelly, L. (1982). Copulation increases offensive attack in male rats. Physiology & Behavior, 29, 381–385.

    Article  CAS  Google Scholar 

  • Flannelly, K., & Lore, R. (1977). The influence of females upon aggression in domesticated male rats (Rattus norvegicus). Animal Behaviour, 25, 654–659.

    Article  PubMed  CAS  Google Scholar 

  • Galef, B. G., Jr., Lim, T. C. W., & Gilbert, G. S. (2008). Evidence of mate choice copying in Norway rats, Rattus norvegicus. Animal Behaviour, 75, 1117–1123.

    Article  Google Scholar 

  • Glaser, R. L., Ramsay, J. P., & Morison, I. M. (2006). The imprinted gene and parent-of-origin effect database now includes parental origin of de novo mutations. Nucleic Acids Research, 34, D29–D31.

    Article  PubMed  CAS  Google Scholar 

  • Glenn, C. C., Driscoll, D. J., Yang, T. P., & Nicholls, R. D. (1997). Genomic imprinting: Potential function and mechanisms revealed by the Prader-Willi and Angelman syndromes. Molecular Human Reproduction, 3, 321–332.

    Article  PubMed  CAS  Google Scholar 

  • Goyens, J., & Noirot, E. (1975). Effects of cohabitation with females on aggressive behavior between male mice. Developmental Psychobiology, 8, 79–84.

    Article  PubMed  CAS  Google Scholar 

  • Haig, D., & Graham, C. (1991). Genomic imprinting and the strange case of the insulin-like growth factor II receptor. Cell, 64, 1045–1046.

    Article  PubMed  CAS  Google Scholar 

  • Hayashi, S., & Kimura, T. (1974). Sex-attractant emitted by female mice. Physiology & Behavior, 13, 563–567.

    Article  CAS  Google Scholar 

  • Heeb, M. M., & Yahr, P. (1996). c-Fos immunoreactivity in the sexually dimorphic area of the hypothalamus and related brain regions of male gerbils after exposure to sex-related stimuli or performance of specific sexual behaviors. Neuroscience, 72, 1049–1071.

    Article  PubMed  CAS  Google Scholar 

  • Hillegaart, V., Alster, P., Uvnäs-Moberg, K., & Ahlenius, S. (1998). Sexual motivation promotes oxytocin secretion in male rats. Peptides, 19, 39–45.

    Article  PubMed  CAS  Google Scholar 

  • Hore, T. A., Rapkins, R. W., & Graves, J. A. M. (2007). Construction and evolution of imprinted loci in mammals. Trends in Genetics, 23, 440–448.

    Article  PubMed  CAS  Google Scholar 

  • Hosokawa, N., & Chiba, A. (2005). Effects of sexual experience on conspecific odor preference and estrous odor-induced activation of the vomeronasal projection pathway and the nucleus accumbens in male rats. Brain Research, 1066, 101–108.

    Article  PubMed  CAS  Google Scholar 

  • Hull, E. M., Bitran, D., Pehek, E. A., Warner, R. K., Band, L. C., & Holmes, G. M. (1986). Dopaminergic control of male sex behavior in rats: Effects of an intracerebrally-infused ­agonist. Brain Research, 370, 73–81.

    Article  PubMed  CAS  Google Scholar 

  • Hull, E. M., Du, J., Lorrain, D. S., & Matuszewich, L. (1995). Extracellular dopamine in the medial preoptic area: Implications for sexual motivation and hormonal control of copulation. The Journal of Neuroscience, 15, 7465–7471.

    PubMed  CAS  Google Scholar 

  • Hurst, L. D., & McVean, G. T. (1997). Growth effects of uniparental disomies and the conflict theory of genomic imprinting. Trends in Genetics, 13, 436.

    Article  PubMed  CAS  Google Scholar 

  • Hurst, L. D., & McVean, G. T. (1998). Do we understand the evolution of genomic imprinting? Current Opinion in Genetics & Development, 8, 701–708.

    Article  CAS  Google Scholar 

  • Illig, K. R., & Haberly, L. B. (2003). Odor-evoked activity is spatially distributed in piriform cortex. The Journal of Comparative Neurology, 457, 361–373.

    Article  PubMed  Google Scholar 

  • Isles, A. R., & Humby, T. (2006). Modes of imprinted gene action in learning disability. Journal of Intellectual Disability Research, 50, 318–325.

    Article  PubMed  CAS  Google Scholar 

  • Jiang, Y.-H., Tsai, T.-F., Bressler, J., & Beaudet, A. L. (1998). Imprinting in Angelman and Prader-Willi syndromes. Current Opinion in Genetics & Development, 8, 334.

    Article  CAS  Google Scholar 

  • Jirikowski, G. F., Caldwell, J. D., Haussler, H. U., & Pedersen, C. A. (1991). Mating alters topography and content of oxytocin immunoreactivity in male mouse brain. Cell and Tissue Research, 266, 399–403.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, M. D., Wu, X. W., Aithmitti, N., & Morrison, R. S. (2002). Peg3 / Pw1 is a mediator between p53 and Bax in DNA damage- induced neuronal death. The Journal of Biological Chemistry, 277, 23000–23007.

    Article  PubMed  CAS  Google Scholar 

  • Kaneko-Ishino, T., Kohda, T., & Ishino, F. (2003). The regulation and biological significance of genomic imprinting in mammals. Journal of Biochemistry, 133, 699–711.

    Article  PubMed  CAS  Google Scholar 

  • Kavaliers, M., Colwell, D. D., & Choleris, E. (1998). Analgesic responses of male mice exposed to the odors of parasitized females: Effects of male sexual experience and infection status. Behavioral Neuroscience, 112, 1001–1011.

    Article  PubMed  CAS  Google Scholar 

  • Keller, M., Douhard, Q., Baum, M. J., & Bakker, J. (2006a). Destruction of the main olfactory epithelium reduces female sexual behavior and olfactory investigation in female mice. Chemical Senses, 31, 315–323.

    Article  PubMed  Google Scholar 

  • Keller, M., Douhard, Q., Baum, M. J., & Bakker, J. (2006b). Sexual experience does not compensate for the disruptive effects of zinc sulfate–lesioning of the main olfactory epithelium on sexual behavior in male mice. Chemical Senses, 31, 753–762.

    Article  PubMed  CAS  Google Scholar 

  • Kelley, A. E. (2004). Ventral striatal control of appetitive motivation: Role in ingestive behavior and reward-related learning. Neuroscience and Biobehavioral Reviews, 27, 765.

    Article  PubMed  Google Scholar 

  • Keverne, E. B. (2001). Genomic imprinting, maternal care, and brain evolution. Hormones and Behavior, 40, 146–155.

    Article  PubMed  CAS  Google Scholar 

  • Keverne, E. B., & Curley, J. P. (2008). Epigenetics, brain evolution and behaviour. Frontiers in Neuroendocrinology, 29, 398–412.

    Article  PubMed  CAS  Google Scholar 

  • Keverne, E. B., Fundele, R., Narasimha, S., Barton, S. C., & Surani, M. A. (1996). Genomic imprinting and the differential roles of parental genomes in brain development. Developmental Brain Research, 92, 91–100.

    Article  PubMed  CAS  Google Scholar 

  • Killian, J. K., Nolan, C. M., Stewart, N., Munday, B. L., Andersen, N. A., Nicol, S., et al. (2001). Monotreme IGF2 expression and ancestral origin of genomic imprinting. The Journal of Experimental Zoology, 291, 205–212.

    Article  PubMed  CAS  Google Scholar 

  • Kim, J., Ashworth, L., Branscomb, E., & Stubbs, L. (1997). The human homolog of a mouse-imprinted gene, Peg3, maps to a zinc finger gene-rich region of human chromosome 19q13.4. Genome Research, 7, 532–540.

    PubMed  CAS  Google Scholar 

  • Kippin, T. E., Talianakis, S., Schattmann, L., Bartholomew, S., & Pfaus, J. G. (1998). Olfactory conditioning of sexual behavior in the male rat (Rattus norvegicus). Journal of Comparative Psychology, 112, 389–399.

    Article  Google Scholar 

  • Kondo, Y. (1992). Lesions of the medial amygdala produce severe impairment of copulatory behavior in sexually inexperienced male rats. Physiology & Behavior, 51, 939–943.

    Article  CAS  Google Scholar 

  • Kuroiwa, Y., Kaneko-Ishino, T., Kagitani, F., Kohda, T., Li, L. L., Tada, M., et al. (1996). Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein. Nature Genetics, 12, 186–190.

    Article  PubMed  CAS  Google Scholar 

  • Larsson, K. (1959). Experience and maturation in the development of sexual behaviour in male puberty rat. Behaviour, 14, 101–107.

    Article  Google Scholar 

  • Larsson, K. (1978). Experiential factors in the development of sexual behaviour. In J. B. Hutchison (Ed.), Biological determinants of sexual behaviour (pp. 55–86). Chichester: Wiley.

    Google Scholar 

  • Lau, M. M., Stewart, C. E., Liu, Z., Bhatt, H., Rotwein, P., & Stewart, C. L. (1994). Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes & Development, 8, 2953–2963.

    Article  CAS  Google Scholar 

  • Leypold, B. G., Yu, C. R., Leinders-Zufall, T., Kim, M. M., Zufall, F., & Axel, R. (2002). Altered sexual and social behaviors in trp2 mutant mice. Proceedings of the National Academy of Sciences of the United States of America, 99, 6376–6381.

    Article  PubMed  CAS  Google Scholar 

  • Li, L., Keverne, E. B., Aparicio, S. A., Ishino, F., Barton, S. C., & Surani, M. A. (1999). Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science, 284, 330–333.

    Article  PubMed  CAS  Google Scholar 

  • Lisk, R. D., & Heimann, J. (1980). The effects of sexual experience and frequency of testing on retention of copulatory behavior following castration in the male hamster. Behavioral and Neural Biology, 28, 156–171.

    Article  PubMed  CAS  Google Scholar 

  • Lopez, H. H., & Ettenberg, A. (2000). Haloperidol challenge during copulation prevents subsequent increase in male sexual motivation. Pharmacology, Biochemistry and Behavior, 67, 387–393.

    Article  CAS  Google Scholar 

  • Lopez, H. H., & Ettenberg, A. (2002a). Exposure to female rats produces differences in c-fos induction between sexually-naive and experienced male rats. Brain Research, 947, 57–66.

    Article  PubMed  CAS  Google Scholar 

  • Lopez, H. H., & Ettenberg, A. (2002b). Sexually conditioned incentives: Attenuation of motivational impact during dopamine receptor antagonism. Pharmacology, Biochemistry and Behavior, 72, 65–72.

    Article  CAS  Google Scholar 

  • Lopez, H. H., Olster, D. H., & Ettenberg, A. (1999). Sexual motivation in the male rat: The role of primary incentives and copulatory experience. Hormones and Behavior, 36, 176–185.

    Article  PubMed  CAS  Google Scholar 

  • Lorrain, D. S., & Hull, E. M. (1993). Nitric oxide increases dopamine and serotonin release in the medial preoptic area. NeuroReport, 5, 87–89.

    Article  PubMed  CAS  Google Scholar 

  • Lorrain, D. S., Matuszewich, L., Howard, R. V., Du, J., & Hull, E. M. (1996). Nitric oxide promotes medial preoptic dopamine release during male rat copulation. NeuroReport, 8, 31–34.

    Article  PubMed  CAS  Google Scholar 

  • Lumley, L. A., & Hull, E. M. (1999). Effects of a D1 antagonist and of sexual experience on copulation-induced Fos-like immunoreactivity in the medial preoptic nucleus. Brain Research, 829, 55–68.

    Article  PubMed  CAS  Google Scholar 

  • Mandiyan, V. S., Coats, J. K., & Shah, N. M. (2005). Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nature Neuroscience, 8, 1660–1662.

    Article  PubMed  CAS  Google Scholar 

  • Manning, A., & Thompson, M. L. (1976). Postcastration retention of sexual behaviour in the male BDF1 mouse: The role of experience. Animal Behaviour, 24, 523–533.

    Article  PubMed  CAS  Google Scholar 

  • Martel, K. L., & Baum, M. J. (2009). A centrifugal pathway to the mouse accessory olfactory bulb from the medial amygdala conveys gender-specific volatile pheromonal signals. The European Journal of Neuroscience, 29, 368–376.

    Article  PubMed  Google Scholar 

  • McGrath, J., & Solter, D. (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell, 37, 179–183.

    Article  PubMed  CAS  Google Scholar 

  • Meredith, M. (1986). Vomeronasal organ removal before sexual experience impairs male hamster mating behavior. Physiology & Behavior, 36, 737–743.

    Article  CAS  Google Scholar 

  • Moore, T., & Haig, D. (1991). Genomic imprinting in mammalian development – a parental ­tug-of-war. Trends in Genetics, 7, 45–49.

    PubMed  CAS  Google Scholar 

  • Moore, T., & Mills, W. (2008). Evolutionary theories of imprinting – enough already! Advances in Experimental Medicine and Biology, 626, 116–122.

    Article  PubMed  Google Scholar 

  • Morison, I. M., Ramsay, J. P., & Spencer, H. G. (2005). A census of mammalian imprinting. Trends in Genetics, 21, 457–465.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, M. R. (1973). Effects of female hamster vaginal discharge on the behavior of male hamsters. Behavioral Biology, 9, 367–375.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, M. R., & Schneider, G. E. (1970). Olfactory bulb removal eliminates mating behavior in the male golden hamster. Science, 167, 302–304.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, S. K., Wylie, A. A., & Jirtle, R. L. (2001). Imprinting of PEG3, the human homologue of a mouse gene involved in nurturing behavior. Genomics, 71, 110–117.

    Article  PubMed  CAS  Google Scholar 

  • Nishitani, S., Moriya, T., Kondo, Y., Sakuma, Y., & Shinohara, K. (2004). Induction of Fos immunoreactivity in oxytocin neurons in the paraventricular nucleus after female odor exposure in male rats: Effects of sexual experience. Cellular and Molecular Neurobiology, 24, 283–291.

    Article  PubMed  Google Scholar 

  • Nunez, A. A., & Tan, D. T. (1984). Courtship ultrasonic vocalizations in male Swiss-Webster mice: Effects of hormones and sexual experience. Physiology & Behavior, 32, 717–721.

    Article  CAS  Google Scholar 

  • Nyby, J., Wysocki, C. J., Whitney, G., & Dizinno, G. (1977). Pheromonal regulation of male mouse ultrasonic courtship (Mus musculus). Animal Behaviour, 25, 333–341.

    Article  PubMed  CAS  Google Scholar 

  • Orr, H. A. (1995). Somatic mutation favors the evolution of diploidy. Genetics, 139, 1441–1447.

    PubMed  CAS  Google Scholar 

  • Pask, A. J., Papenfuss, A. T., Ager, E. I., McColl, K. A., Speed, T. P., & Renfree, M. B. (2009). Analysis of the platypus genome suggests a transposon origin for mammalian imprinting. Genome Biology, 10, R1.

    Article  PubMed  CAS  Google Scholar 

  • Pfaus, J. G., Damsma, G., Nomikos, G. G., Wenkstern, D. G., Blaha, C. D., Phillips, A. G., et al. (1990). Sexual behavior enhances central dopamine transmission in the male rat. Brain Research, 530, 345–348.

    Article  PubMed  CAS  Google Scholar 

  • Pfaus, J. G., & Phillips, A. G. (1991). Role of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat. Behavioral Neuroscience, 105, 727–743.

    Article  PubMed  CAS  Google Scholar 

  • Pfeiffer, C. A., & Johnston, R. E. (1994). Hormonal and behavioral responses of male hamsters to females and female odors: Roles of olfaction, the vomeronasal system, and sexual experience. Physiology & Behavior, 55, 129–138.

    Article  CAS  Google Scholar 

  • Powers, J. B., & Winans, S. S. (1975). Vomeronasal organ: Critical role in mediating sexual behavior of the male hamster. Science, 187, 961–963.

    Article  PubMed  CAS  Google Scholar 

  • Rastogi, R. K., Milone, M., & Chieffi, G. (1981). Impact of socio-sexual conditions on the epididymis and fertility in the male mouse. Journal of Reproduction and Fertility, 63, 331–334.

    Article  PubMed  CAS  Google Scholar 

  • Reik, W., Constancia, M., Fowden, A., Anderson, N., Dean, W., Ferguson-Smith, A., et al. (2003). Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. The Journal of Physiology, 547, 35–44.

    Article  CAS  Google Scholar 

  • Relaix, F., Wei, X. J., Li, W., Pan, J. J., Lin, Y. H., Bowtell, D. D., et al. (2000). Pw1 / Peg3 is a potential cell death mediator and cooperates with Siah1a in p53-mediated apoptosis. Proceedings of the National Academy of Sciences of the United States of America, 97, 2105–2110.

    Article  PubMed  CAS  Google Scholar 

  • Relaix, F., Weng, X., Marazzi, G., Yang, E., Copeland, N., Jenkins, N., et al. (1996). Pw1, a novel zinc finger gene implicated in the myogenic and neuronal lineages. Developmental Biology, 177, 383–396.

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Manzo, G., Lopez-Rubalcava, C., & Fernandez-Guasti, A. (1999). Anxiolytic-like effect of ejaculation under various sexual behavior conditions in the male rat. Physiology & Behavior, 67, 651–657.

    Article  CAS  Google Scholar 

  • Sahoo, T., del Gaudio, D., German, J. R., Shinawi, M., Peters, S. U., Person, R. E., et al. (2008). Prader-Willi phenotype caused by paternal deficiency for the HBII-85 C/D box small nucleolar RNA cluster. Nature Genetics, 40, 719–721.

    Article  PubMed  CAS  Google Scholar 

  • Sipos, M. L., Kerchner, M., & Nyby, J. G. (1992). An ephemeral sex pheromone in the urine of female house mice (Mus domesticus). Behavioral and Neural Biology, 58, 138–143.

    Article  PubMed  CAS  Google Scholar 

  • Sipos, M. L., Wysocki, C. J., Nyby, J. G., Wysocki, L., & Nemura, T. A. (1995). An ephemeral pheromone of female house mice: Perception via the main and accessory olfactory systems. Physiology & Behavior, 58, 529–534.

    Article  CAS  Google Scholar 

  • Sleutels, F., Barlow, D. P., & Lyle, R. (2000). The uniqueness of the imprinting mechanism. Current Opinion in Genetics & Development, 10, 229–233.

    Article  CAS  Google Scholar 

  • Solter, D. (1988). Differential imprinting and expression of maternal and paternal genomes. Annual Review of Genetics, 22, 127–146.

    Article  PubMed  CAS  Google Scholar 

  • Spahn, L., & Barlow, D. P. (2003). An ICE pattern crystallizes. Nature Genetics, 35, 11–12.

    Article  PubMed  CAS  Google Scholar 

  • Steel, E., & Keverne, E. B. (1985). Effect of female odour on male hamsters mediated by the vomeronasal organ. Physiology & Behavior, 35, 195–200.

    Article  CAS  Google Scholar 

  • Stern, J. J. (1970). Responses of male rats to sex odors. Physiology & Behavior, 5, 519–524.

    Article  CAS  Google Scholar 

  • Stowers, L., Holy, T. E., Meister, M., Dulac, C., & Koentges, G. (2002). Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science, 295, 1493–1500.

    Article  PubMed  CAS  Google Scholar 

  • Surani, M. A. (1998). Imprinting and the initiation of gene silencing in the germ line. Cell, 93, 309.

    Article  PubMed  CAS  Google Scholar 

  • Surani, M. A., Barton, S. C., & Norris, M. L. (1984). Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature, 308, 548–550.

    Article  PubMed  CAS  Google Scholar 

  • Surani, M. A. H., Barton, S. C., & Norris, M. L. (1986). Nuclear transplantation in the mouse: Heritable differences between parental genomes after activation of the embryonic genome. Cell, 45, 127–136.

    Article  PubMed  CAS  Google Scholar 

  • Suzuki, S., Renfree, M. B., Pask, A. J., Shaw, G., Kobayashi, S., Kohda, T., et al. (2005). Genomic imprinting of IGF2, p57KIP2 and PEG1/MEST in a marsupial, the tammar wallaby. Mechanisms of Development, 122, 213–222.

    Article  PubMed  CAS  Google Scholar 

  • Swaney, W. T., Curley, J. P., Champagne, F. A., & Keverne, E. B. (2007). Genomic imprinting mediates sexual experience-dependent olfactory learning in male mice. Proceedings of the National Academy of Sciences of the United States of America, 104, 6084–6089.

    Article  PubMed  CAS  Google Scholar 

  • Swaney, W. T., Curley, J. P., Champagne, F. A., & Keverne, E. B. (2008). The paternally expressed gene Peg3 regulates sexual experience-dependent preferences for estrous odors. Behavioral Neuroscience, 122, 963–973.

    Article  PubMed  Google Scholar 

  • Thorvaldsen, J. L., Duran, K. L., & Bartolomei, M. S. (1998). Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes & Development, 12, 3693–3702.

    Article  CAS  Google Scholar 

  • Tycko, B., & Morison, I. M. (2002). Physiological functions of imprinted genes. Journal of Cellular Physiology, 192, 245–258.

    Article  PubMed  CAS  Google Scholar 

  • Valenstein, E. S., & Goy, R. W. (1957). Further studies of the organization and display of sexual behavior in male guinea pigs. Journal of Comparative and Physiological Psychology, 50, 115–119.

    Article  PubMed  CAS  Google Scholar 

  • Valenstein, E. S., Riss, W., & Young, W. C. (1955). Experiential and genetic factors in the organization of sexual behavior in male guinea pigs. Journal of Comparative and Physiological Psychology, 48, 397–403.

    Article  PubMed  CAS  Google Scholar 

  • Varmuza, S., & Mann, M. (1994). Genomic imprinting – defusing the ovarian time bomb. Trends in Genetics, 10, 118–123.

    Article  PubMed  CAS  Google Scholar 

  • Warner, R. K., Thompson, J. T., Markowski, V. P., Loucks, J. A., Bazzett, T. J., Eaton, R. C., et al. (1991). Microinjection of the dopamine antagonist cis-flupenthixol into the MPOA impairs copulation, penile reflexes and sexual motivation in male rats. Brain Research, 540, 177–182.

    Article  PubMed  CAS  Google Scholar 

  • Warren, W. C., Hillier, L. W., Marshall Graves, J. A., Birney, E., Ponting, C. P., Grutzner, F., et al. (2008). Genome analysis of the platypus reveals unique signatures of evolution. Nature, 453, 175–183.

    Article  PubMed  CAS  Google Scholar 

  • Watts, P. C., Buley, K. R., Sanderson, S., Boardman, W., Ciofi, C., & Gibson, R. (2006). Parthenogenesis in Komodo dragons. Nature, 444, 1021–1022.

    Article  PubMed  CAS  Google Scholar 

  • Wenkstern, D., Pfaus, J. G., & Fibiger, H. C. (1993). Dopamine transmission increases in the nucleus accumbens of male rats during their first exposure to sexually receptive female rats. Brain Research, 618, 41–46.

    Article  PubMed  CAS  Google Scholar 

  • Whittington, J., Holland, A., Webb, T., Butler, J., Clarke, D., & Boer, H. (2004). Cognitive abilities and genotype in a population-based sample of people with Prader-Willi syndrome. Journal of Intellectual Disability Research, 48, 172–187.

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson, L. S., Davies, W., & Isles, A. R. (2007). Genomic imprinting effects on brain development and function. Nature Reviews. Neuroscience, 8, 832–843.

    Article  PubMed  CAS  Google Scholar 

  • Williamson, C. M., Ball, S. T., Nottingham, W. T., Skinner, J. A., Plagge, A., Turner, M. D., et al. (2004). A cis-acting control region is required exclusively for the tissue-specific imprinting of Gnas. Nature Genetics, 36, 894.

    Article  PubMed  CAS  Google Scholar 

  • Williamson, C. M., Turner, M. D., Ball, S. T., Nottingham, W. T., Glenister, P., Fray, M., et al. (2006). Identification of an imprinting control region affecting the expression of all transcripts in the Gnas cluster. Nature Genetics, 38, 350–355.

    Article  PubMed  CAS  Google Scholar 

  • Witt, D. M., & Insel, T. R. (1994). Increased Fos expression in oxytocin neurons following ­masculine sexual behavior. Journal of Neuroendocrinology, 6, 13–18.

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi, A., Taniguchi, M., Hori, O., Ogawa, S., Tojo, N., Matsuoka, N., et al. (2002). Peg3/Pw1 is involved in p53-mediated cell death pathway in brain ischemia/hypoxia. The Journal of Biological Chemistry, 277, 623–629.

    Article  PubMed  CAS  Google Scholar 

  • Yoon, H., Enquist, L. W., & Dulac, C. (2005). Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell, 123, 669–682.

    Article  PubMed  CAS  Google Scholar 

  • Zufall, F., & Leinders-Zufall, T. (2007). Mammalian pheromone sensing. Current Opinion in Neurobiology, 17, 483–489.

    Article  PubMed  CAS  Google Scholar 

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Swaney, W.T., Keverne, E.B. (2011). Genomic Imprinting and Sexual Experience-Dependent Learning in the Mouse. In: Clelland, J. (eds) Genomics, Proteomics, and the Nervous System. Advances in Neurobiology, vol 2. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-7197-5_8

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