Innate and learned aspects of pheromone-mediated social behaviours

Animal Behaviour

Volumn 97, Issue , 2014, Pages 301-311

  Beny, Yamit ^a   Kimchi, Tali ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Associative learning; Dopamine; Innate behaviour; Main olfactory epithelium; Neural pathway; Pheromones; Reproductive behaviour; Reward value; Rodents; Vomeronasal organ

Indexed keywords

BEHAVIORAL RESPONSE; ENVIRONMENTAL CONDITIONS; INNATE BEHAVIOR; LEARNING; MAMMAL; OLFACTION; PHEROMONE; REPRODUCTIVE BEHAVIOR; SOCIAL BEHAVIOR;

RODENTIA;

EID: 84908622300     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2014.09.014     Document Type: Article

References (182)

1. Agustin-Pavon C., Martinez-Ricos J., Martinez-Garcia F., Lanuza E. Effects of dopaminergic drugs on innate pheromone-mediated reward in female mice: a new case of dopamine-independent "liking.". Behavioral Neuroscience 2007, 121(5):920-932. 10.1037/0735-7044.121.5.920.
2. Alcock J. Animal behavior: An evolutionary approach 2013, Sinauer, Sunderland, MA. 10th ed.
3. Anderson D.J. Optogenetics, sex, and violence in the brain: implications for psychiatry. Biological Psychiatry 2012, 71(12):1081-1089. 10.1016/j.biopsych.2011.11.012.
4. Anderson P., Hansson B.S., Nilsson U., Han Q., Sjoholm M., Skals N., et al. Increased behavioral and neuronal sensitivity to sex pheromone after brief odor experience in a moth. Chemical Senses 2007, 32(5):483-491. 10.1093/chemse/bjm017.
5. Argiolas A., Melis M.R. Neuropeptides and central control of sexual behaviour from the past to the present: a review. Progress in Neurobiology 2013, 108:80-107. 10.1016/j.pneurobio.2013.06.006.
6. Ball G.F., Balthazart J. How useful is the appetitive and consummatory distinction for our understanding of the neuroendocrine control of sexual behavior?. Hormones and Behavior 2008, 53(2):307-311. 10.1016/j.yhbeh.2007.09.023.
7. Baxi K.N., Dorries K.M., Eisthen H.L. Is the vomeronasal system really specialized for detecting pheromones?. Trends in Neurosciences 2006, 29(1):1-7. 10.1016/j.tins.2005.10.002.
8. Bell M.R., De Lorme K.C., Figueira R.J., Kashy D.A., Sisk C.L. Adolescent gain in positive valence of a socially relevant stimulus: engagement of the mesocorticolimbic reward circuitry. The European Journal of Neuroscience 2013, 37(3):457-468. 10.1111/ejn.12058.
9. Ben-Shaul Y., Katz L.C., Mooney R., Dulac C. Invivo vomeronasal stimulation reveals sensory encoding of conspecific and allospecific cues by the mouse accessory olfactory bulb. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(11):5172-5177. 10.1073/pnas.0915147107.
10. Bergan J.F., Ben-Shaul Y., Dulac C. Sex-specific processing of social cues in the medial amygdala. eLife 2014, 3:e02743. 10.7554/eLife.02743.
11. Berridge K.C. Reward learning: reinforcement, incentives, and expectations. Psychology of learning and motivation: Advances in research and theory 2000, Vol. 40:223-278. Academic Press, San Diego, CA.
12. Beynon R.J., Hurst J.L. Urinary proteins and the modulation of chemical scents in mice and rats. Peptides 2004, 25(9):1553-1563. 10.1016/j.peptides.2003.12.025.
13. Brechbuhl J., Klaey M., Broillet M.C. Grueneberg ganglion cells mediate alarm pheromone detection in mice. Science 2008, 321(5892):1092-1095. 10.1126/science.1160770.
14. Brechbuhl J., Moine F., Klaey M., Nenniger-Tosato M., Hurni N., Sporkert F., et al. Mouse alarm pheromone shares structural similarity with predator scents. Proceedings of the National Academy of Sciences of the United States of America 2013, 110(12):4762-4767. 10.1073/pnas.1214249110.
15. Brennan P.A., Keverne E.B. Neural mechanisms of mammalian olfactory learning. Progress in Neurobiology 1997, 51(4):457-481.
16. Brennan P.A., Keverne E.B. Something in the air? New insights into mammalian pheromones. Current Biology 2004, 14(2):R81-R89.
17. Brennan P.A., Zufall F. Pheromonal communication in vertebrates. Nature 2006, 444(7117):308-315. 10.1038/nature05404.
18. Bridges R.S. Aquantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology 1984, 114(3):930-940. 10.1210/endo-114-3-930.
19. Bridges R.S., Ronsheim P.M. Prolactin (PRL) regulation of maternal behavior in rats: bromocriptine treatment delays and PRL promotes the rapid onset of behavior. Endocrinology 1990, 126(2):837-848. 10.1210/endo-126-2-837.
20. Brischoux F., Chakraborty S., Brierley D.I., Ungless M.A. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(12):4894-4899. 10.1073/pnas.0811507106.
21. Brouette-Lahlou I., Godinot F., Vernet-Maury E. The mother rat's vomeronasal organ is involved in detection of dodecyl propionate, the pup's preputial gland pheromone. Physiology and Behavior 1999, 66(3):427-436.
22. Brown R.E. Odor preference and urine-marking scales in male and female rats: effects of gonadectomy and sexual experience on responses to conspecific odors. Journal of Comparative and Physiological Psychology 1977, 91(5):1190.
23. Buron G., Hacquemand R., Pourie G., Lucarz A., Jacquot L., Brand G. Comparative behavioral effects between synthetic 2,4,5-trimethylthiazoline (TMT) and the odor of natural fox (Vulpes vulpes) feces in mice. Behavioral Neuroscience 2007, 121(5):1063-1072. 10.1037/0735-7044.121.5.1063.
24. Cádiz-Moretti B., Martínez-García F., Lanuza E. Neural substrate to associate odorants and pheromones: convergence of projections from the main and accessory olfactory bulbs in mice. Chemical signals in vertebrates 12 2013, 3-16. Springer, New York. M.L. East, M. Dehnhard (Eds.).
25. Cartwright J. Evolution and human behavior: Darwinian perspectives on human nature 2000, The MIT Press, Cambridge, MA.
26. Celsi F., D'Errico A., Menini A. Responses to sulfated steroids of female mouse vomeronasal sensory neurons. Chemical Senses 2012, 37(9):849-858. 10.1093/chemse/bjs068.
27. Chalfin L., Dayan M., Levy D.R., Austad S.N., Miller R.A., Iraqi F.A., et al. Mapping ecologically relevant social behaviours by gene knockout in wild mice. Nature Communications 2014, 5(4569). 10.1038/ncomms5569.
28. Chamero P., Leinders-Zufall T., Zufall F. From genes to social communication: molecular sensing by the vomeronasal organ. Trends in Neurosciences 2012, 35(10):597-606. 10.1016/j.tins.2012.04.011.
29. Chamero P., Marton T.F., Logan D.W., Flanagan K., Cruz J.R., Saghatelian A., et al. Identification of protein pheromones that promote aggressive behaviour. Nature 2007, 450(7171):899-902. 10.1038/nature05997.
30. Charra R., Datiche F., Casthano A., Gigot V., Schaal B., Coureaud G. Brain processing of the mammary pheromone in newborn rabbits. Behavioural Brain Research 2012, 226(1):179-188. 10.1016/j.bbr.2011.09.008.
31. Cheetham S.A., Thom M.D., Jury F., Ollier W.E., Beynon R.J., Hurst J.L. The genetic basis of individual-recognition signals in the mouse. Current Biology 2007, 17(20):1771-1777. 10.1016/j.cub.2007.10.007.
32. Choi G.B., Dong H.W., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., Swanson L.W., et al. Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 2005, 46(4):647-660. 10.1016/j.neuron.2005.04.011.
33. Connor J. Olfactory control of aggressive and sexual behavior in the mouse (Mus musculus L.). Psychonomic Science 1972, 27(1):1-3.
34. Coppola D.M., O'Connell R.J. Are pheromones their own reward?. Physiology and Behavior 1988, 44(6):811-816.
35. Coureaud G., Moncomble A.S., Montigny D., Dewas M., Perrier G., Schaal B. Apheromone that rapidly promotes learning in the newborn. Current Biology 2006, 16(19):1956-1961.
36. Damsma G., Pfaus J.G., Wenkstern D., Phillips A.G., Fibiger H.C. Sexual behavior increases dopamine transmission in the nucleus accumbens and striatum of male rats: comparison with novelty and locomotion. Behavioral Neuroscience 1992, 106(1):181-191.
37. Davies N.B., Krebs J.R. Behavioural ecology: An evolutionary approach 1997, Blackwell Scientific, Cambridge, MA. 4th ed.
38. Del Punta K., Leinders-Zufall T., Rodriguez I., Jukam D., Wysocki C.J., Ogawa S., et al. Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 2002, 419(6902):70-74. 10.1038/nature00955.
39. Dewan A., Pacifico R., Zhan R., Rinberg D., Bozza T. Non-redundant coding of aversive odours in the main olfactory pathway. Nature 2013, 497(7450):486-489. 10.1038/nature12114.
40. Dizinno G., Whitney G., Nyby J. Ultrasonic vocalizations by male mice (Mus musculus) to female sex pheromone: experiential determinants. Behavioral Biology 1978, 22(1):104-113.
41. Doty R.L. The great pheromone myth 2010, Johns Hopkins University Press, Baltimore, MD.
42. Dudareva N.A., Pichersky E. Biology of floral scent 2006, CRC Press, Boca Raton, FL.
43. Dukas R. Evolutionary biology of insect learning. Annual Review of Entomology 2008, 53:145-160. 10.1146/annurev.ento.53.103106.093343.
44. Dulac C., Kimchi T. Neural mechanisms underlying sex-specific behaviors in vertebrates. Current Opinion in Neurobiology 2007, 17(6):675-683. 10.1016/j.conb.2008.01.009.
45. Dulac C., Torello A.T. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nature Reviews Neuroscience 2003, 4(7):551-562. 10.1038/nrn1140.
46. Dulac C., Wagner S. Genetic analysis of brain circuits underlying pheromone signaling. Annual Review of Genetics 2006, 40:449-467. 10.1146/annurev.genet.39.073003.093937.
47. Ejima A., Smith B.P., Lucas C., Levine J.D., Griffith L.C. Sequential learning of pheromonal cues modulates memory consolidation in trainer-specific associative courtship conditioning. Current Biology 2005, 15(3):194-206. 10.1016/j.cub.2005.01.035.
48. Ejima A., Smith B.P., Lucas C., van der Goes van Naters W., Miller C.J., Carlson J.R., et al. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Current Biology 2007, 17(7):599-605. 10.1016/j.cub.2007.01.053.
49. Everitt B.J., Cador M., Robbins T.W. Interactions between the amygdala and ventral striatum in stimulus-reward associations: studies using a second-order schedule of sexual reinforcement. Neuroscience 1989, 30(1):63-75.
50. Everitt B.J., Fray P., Kostarczyk E., Taylor S., Stacey P. Studies of instrumental behavior with sexual reinforcement in male rats (Rattus norvegicus): I. Control by brief visual stimuli paired with a receptive female. Journal of Comparative Psychology 1987, 101(4):395-406.
51. Fahrbach S.E., Morrell J.I., Pfaff D.W. Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Hormones and Behavior 1984, 18(3):267-286.
52. Ferrero D.M., Lemon J.K., Fluegge D., Pashkovski S.L., Korzan W.J., Datta S.R., et al. Detection and avoidance of a carnivore odor by prey. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(27):11235-11240. 10.1073/pnas.1103317108.
53. Ferrero D.M., Moeller L.M., Osakada T., Horio N., Li Q., Roy D.S., et al. Ajuvenile mouse pheromone inhibits sexual behaviour through the vomeronasal system. Nature 2013, 502(7471):368-371. 10.1038/nature12579.
54. Floresco S.B., Yang C.R., Phillips A.G., Blaha C.D. Basolateral amygdala stimulation evokes glutamate receptor-dependent dopamine efflux in the nucleus accumbens of the anaesthetized rat. The European Journal of Neuroscience 1998, 10(4):1241-1251.
55. Garratt M., Stockley P., Armstrong S.D., Beynon R.J., Hurst J.L. The scent of senescence: sexual signalling and female preference in house mice. Journal of Evolutionary Biology 2011, 24(11):2398-2409. 10.1111/j.1420-9101.2011.02367.x.
56. Gelstein S., Yeshurun Y., Rozenkrantz L., Shushan S., Frumin I., Roth Y., et al. Human tears contain a chemosignal. Science 2011, 331(6014):226-230. 10.1126/science.1198331.
57. Giannetti N., Saucier D., Astic L. Organization of the septal organ projection to the main olfactory bulb in adult and newborn rats. The Journal of Comparative Neurology 1992, 323(2):288-298. 10.1002/cne.903230211.
58. Graham J.M., Desjardins C. Classical conditioning: induction of luteinizing hormone and testosterone secretion in anticipation of sexual activity. Science 1980, 210(4473):1039-1041.
59. Greenfield M.D. Moth sex pheromones: an evolutionary perspective. Florida Entomologist 1981, 64(1):4-17.
60. Grosser B.I., Monti-Bloch L., Jennings-White C., Berliner D.L. Behavioral and electrophysiological effects of androstadienone, a human pheromone. Psychoneuroendocrinology 2000, 25(3):289-299.
61. Grüneberg H. Aganglion probably belonging to the N. terminalis system in the nasal mucosa of the mouse. Zeitschrift für Anatomie und Entwicklungsgeschichte 1973, 140(1):39-52.
62. Gutierrez-Castellanos N., Pardo-Bellver C., Martinez-Garcia F., Lanuza E. The vomeronasal cortex - afferent and efferent projections of the posteromedial cortical nucleus of the amygdala in mice. The European Journal of Neuroscience 2014, 39(1):141-158. 10.1111/ejn.12393.
63. Haga-Yamanaka S., Ma L., He J., Qiu Q., Lavis L.D., Looger L.L., et al. Integrated action of pheromone signals in promoting courtship behavior in male mice. eLife 2014, 10.7554/eLife.03025.
64. Haga S., Hattori T., Sato T., Sato K., Matsuda S., Kobayakawa R., et al. The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 2010, 466(7302):118-122. 10.1038/nature09142.
65. Harding S.M., McGinnis M.Y. Effects of testosterone in the VMN on copulation, partner preference, and vocalizations in male rats. Hormones and Behavior 2003, 43(2):327-335.
66. Harding S.M., Velotta J.P. Comparing the relative amount of testosterone required to restore sexual arousal, motivation, and performance in male rats. Hormones and Behavior 2011, 59(5):666-673. 10.1016/j.yhbeh.2010.09.009.
67. Hastings M., O'Neill J.S., Maywood E.S. Circadian clocks: regulators of endocrine and metabolic rhythms. The Journal of Endocrinology 2007, 195(2):187-198. 10.1677/JOE-07-0378.
68. He J., Ma L., Kim S., Nakai J., Yu C.R. Encoding gender and individual information in the mouse vomeronasal organ. Science 2008, 320(5875):535-538. 10.1126/science.1154476.
69. Hosokawa N., Chiba A. 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 2005, 1066(1-2):101-108. 10.1016/j.brainres.2005.10.036.
70. Hosokawa N., Chiba A. Effects of sexual experience on conspecific odor preference and male odor-induced activation of the vomeronasal projection pathway and the nucleus accumbens in female rats. Brain Research 2007, 1175:66-75. 10.1016/j.brainres.2007.07.071.
71. Hull E.M., Lorrain D.S., Du J., Matuszewich L., Lumley L.A., Putnam S.K., et al. Hormone-neurotransmitter interactions in the control of sexual behavior. Behavioural Brain Research 1999, 105(1):105-116.
72. Hurst J.L. Female recognition and assessment of males through scent. Behavioural Brain Research 2009, 200(2):295-303. 10.1016/j.bbr.2008.12.020.
73. Hurst J.L., Beynon R.J. Scent wars: the chemobiology of competitive signalling in mice. Bioessays 2004, 26(12):1288-1298. 10.1002/bies.20147.
74. Isogai Y., Si S., Pont-Lezica L., Tan T., Kapoor V., Murthy V.N., et al. Molecular organization of vomeronasal chemoreception. Nature 2011, 478(7368):241-245. 10.1038/nature10437.
75. Jemiolo B., Alberts J., Sochinski-Wiggins S., Harvey S., Novotny M. Behavioural and endocrine responses of female mice to synthetic analogues of volatile compounds in male urine. Animal Behaviour 1985, 33(4):1114-1118.
76. Jemiolo B., Harvey S., Novotny M. Promotion of the Whitten effect in female mice by synthetic analogs of male urinary constituents. Proceedings of the National Academy of Sciences of the United States of America 1986, 83(12):4576-4579.
77. Jemiolo B., Xie T.M., Novotny M. Socio-sexual olfactory preference in female mice: attractiveness of synthetic chemosignals. Physiology and Behavior 1991, 50(6):1119-1122.
78. Johnston R.E., Zahorik D.M. Taste aversions to sexual attractants. Science 1975, 189(4206):893-894.
79. Jones J.L., Day J.J., Aragona B.J., Wheeler R.A., Wightman R.M., Carelli R.M. Basolateral amygdala modulates terminal dopamine release in the nucleus accumbens and conditioned responding. Biological Psychiatry 2010, 67(8):737-744. 10.1016/j.biopsych.2009.11.006.
80. Jones R., Nowell N. Aversive effects of the urine of a male mouse upon the investigatory behaviour of its defeated opponent. Animal Behaviour 1973, 21(4):707-710.
81. Kang N., Baum M.J., Cherry J.A. Adirect main olfactory bulb projection to the 'vomeronasal' amygdala in female mice selectively responds to volatile pheromones from males. The European Journal of Neuroscience 2009, 29(3):624-634. 10.1111/j.1460-9568.2009.06638.x.
82. Kavaliers M., Choleris E., Agmo A., Pfaff D.W. Olfactory-mediated parasite recognition and avoidance: linking genes to behavior. Hormones and Behavior 2004, 46(3):272-283. 10.1016/j.yhbeh.2004.03.005.
83. Kay E., Nyby J. Licl aversive-conditioning has transitory effects on pheromonal responsiveness in male house mice (Mus domesticus). Physiology and Behavior 1992, 52(1):105-113. 10.1016/0031-9384(92)90439-9.
84. Keller M., Baum M.J., Brock O., Brennan P.A., Bakker J. The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behavioural Brain Research 2009, 200(2):268-276.
85. Keller M., Pierman S., Douhard Q., Baum M.J., Bakker J. The vomeronasal organ is required for the expression of lordosis behaviour, but not sex discrimination in female mice. The European Journal of Neuroscience 2006, 23(2):521-530. 10.1111/j.1460-9568.2005.04589.x.
86. Kikusui T., Takigami S., Takeuchi Y., Mori Y. Alarm pheromone enhances stress-induced hyperthermia in rats. Physiology and Behavior 2001, 72(1-2):45-50.
87. Kimchi T., Xu J., Dulac C. Afunctional circuit underlying male sexual behaviour in the female mouse brain. Nature 2007, 448(7157):1009-1014. 10.1038/nature06089.
88. Kimoto H., Haga S., Sato K., Touhara K. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 2005, 437(7060):898-901. 10.1038/nature04033.
89. Knaden M., Hansson B.S. Mapping odor valence in the brain of flies and mice. Current Opinion in Neurobiology 2014, 24(1):34-38. 10.1016/j.conb.2013.08.010.
90. Kobayakawa K., Kobayakawa R., Matsumoto H., Oka Y., Imai T., Ikawa M., et al. Innate versus learned odour processing in the mouse olfactory bulb. Nature 2007, 450(7169):503-508. 10.1038/nature06281.
91. Kobayashi T., Kiyokawa Y., Takeuchi Y., Mori Y. Pretreatment with CP-154526 blocks the modifying effects of alarm pheromone on components of sexual behavior in male, but not in female, rats. Chemical Senses 2011, 36(7):623-632. 10.1093/chemse/bjr017.
92. Korzan W.J., Freamat M., Johnson A.G., Cherry J.A., Baum M.J. Either main or accessory olfactory system signaling can mediate the rewarding effects of estrous female chemosignals in sexually naive male mice. Behavioral Neuroscience 2013, 127(5):755.
93. Leadbeater E., Chittka L. Social learning in insects - from miniature brains to consensus building. Current Biology 2007, 17(16):R703-R713. 10.1016/j.cub.2007.06.012.
94. LeDoux J.E. Emotion circuits in the brain. Annual Review of Neuroscience 2000, 23:155-184. 10.1146/annurev.neuro.23.1.155.
95. Lehrman D.S. Acritique of Konrad Lorenz's theory of instinctive behavior. The Quarterly Review of Biology 1953, 28(4):337-363.
96. Leinders-Zufall T., Brennan P., Widmayer P., S P.C., Maul-Pavicic A., Jager M., et al. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 2004, 306(5698):1033-1037. 10.1126/science.1102818.
97. Leinders-Zufall T., Lane A.P., Puche A.C., Ma W., Novotny M.V., Shipley M.T., et al. Ultrasensitive pheromone detection by mammalian vomeronasal neurons. Nature 2000, 405(6788):792-796. 10.1038/35015572.
98. Leon M., Moltz H. Maternal pheromone: discrimination by pre-weanling albino rats. Physiology and Behavior 1971, 7(2):265-267.
99. Leypold B.G., Yu C.R., Leinders-Zufall T., Kim M.M., Zufall F., Axel R. Altered sexual and social behaviors in trp2 mutant mice. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(9):6376-6381. 10.1073/pnas.082127599.
100. Li Q., Korzan W.J., Ferrero D.M., Chang R.B., Roy D.S., Buchi M., et al. Synchronous evolution of an odor biosynthesis pathway and behavioral response. Current Biology 2013, 23(1):11-20. 10.1016/j.cub.2012.10.047.
101. Liberles S.D. Mammalian pheromones. Annual Review of Physiology 2014, 76:151-175. 10.1146/annurev-physiol-021113-170334.
102. Liberles S.D., Buck L.B. Asecond class of chemosensory receptors in the olfactory epithelium. Nature 2006, 442(7103):645-650. 10.1038/nature05066.
103. Liberles S.D., Horowitz L.F., Kuang D., Contos J.J., Wilson K.L., Siltberg-Liberles J., et al. Formyl peptide receptors are candidate chemosensory receptors in the vomeronasal organ. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(24):9842-9847. 10.1073/pnas.0904464106.
104. Lin D.Y., Zhang S.Z., Block E., Katz L.C. Encoding social signals in the mouse main olfactory bulb. Nature 2005, 434(7032):470-477. 10.1038/nature03414.
105. Logan D.W., Brunet L.J., Webb W.R., Cutforth T., Ngai J., Stowers L. Learned recognition of maternal signature odors mediates the first suckling episode in mice. Current Biology 2012, 22(21):1998-2007. 10.1016/j.cub.2012.08.041.
106. Lorenz K. Der Kumpan in der Umwelt des Vogels. Journal of Ornithology 1935, 83(3):289-413.
107. Lorenz K. The comparative method in studying innate behavior patterns. Society for Experimental Biology 1950, 4:221-268.
108. Lydell K., Doty R.L. Male rat of odor preferences for female urine as a function of sexual experience, urine age, and urine source. Hormones and Behavior 1972, 3(3):205-212.
109. Ma M., Grosmaitre X., Iwema C.L., Baker H., Greer C.A., Shepherd G.M. Olfactory signal transduction in the mouse septal organ. The Journal of Neuroscience 2003, 23(1):317-324.
110. Mackintosh J. Territory formation by laboratory mice. Animal Behaviour 1970, 18:177-183.
111. Malkesman O., Scattoni M.L., Paredes D., Tragon T., Pearson B., Shaltiel G., et al. The female urine sniffing test: a novel approach for assessing reward-seeking behavior in rodents. Biological Psychiatry 2010, 67(9):864-871.
112. Mandiyan V.S., Coats J.K., Shah N.M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nature Neuroscience 2005, 8(12):1660-1662. 10.1038/nn1589.
113. Mannella F., Gurney K., Baldassarre G. The nucleus accumbens as a nexus between values and goals in goal-directed behavior: a review and a new hypothesis. Frontiers in Behavioral Neuroscience 2013, 7:135. 10.3389/fnbeh.2013.00135.
114. Martinez-Garcia F., Martinez-Ricos J., Agustin-Pavon C., Martinez-Hernandez J., Novejarque A., Lanuza E. Refining the dual olfactory hypothesis: pheromone reward and odour experience. Behavioural Brain Research 2009, 200(2):277-286. 10.1016/j.bbr.2008.10.002.
115. Martinez-Hernandez J., Lanuza E., Martinez-Garcia F. Selective dopaminergic lesions of the ventral tegmental area impair preference for sucrose but not for male sexual pheromones in female mice. The European Journal ofNeuroscience 2006, 24(3):885-893. 10.1111/j.1460-9568.2006.04944.x.
116. Martinez-Hernandez J., Lanuza E., Martinez-Garcia F. Lesions of the dopaminergic innervation of the nucleus accumbens medial shell delay the generation of preference for sucrose, but not of sexual pheromones. Behavioural Brain Research 2012, 226(2):538-547. 10.1016/j.bbr.2011.10.013.
117. Matsumoto M., Hikosaka O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 2009, 459(7248):837-841. 10.1038/nature08028.
118. Meeks J.P., Arnson H.A., Holy T.E. Representation and transformation of sensory information in the mouse accessory olfactory system. Nature Neuroscience 2010, 13(6):723-730. 10.1038/nn.2546.
119. Menda G., Uhr J.H., Wyttenbach R.A., Vermeylen F.M., Smith D.M., Harrington L.C., et al. Associative learning in the dengue vector mosquito, Aedes aegypti: avoidance of a previously attractive odor or surface color that is paired with an aversive stimulus. The Journal of Experimental Biology 2013, 216(Pt 2):218-223. 10.1242/jeb.074898.
120. Merton D.V., Morris R.B., Atkinson I.A. Lek behaviour in a parrot: the kakapo Strigops habroptilus of New Zealand. Ibis 1984, 126(3):277-283.
121. Mirenowicz J., Schultz W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 1996, 379(6564):449-451. 10.1038/379449a0.
122. Moncho-Bogani J., Lanuza E., Hernandez A., Novejarque A., Martinez-Garcia F. Attractive properties of sexual pheromones in mice: innate or learned?. Physiology and Behavior 2002, 77(1):167-176.
123. Moncho-Bogani J., Martinez-Garcia F., Novejarque A., Lanuza E. Attraction to sexual pheromones and associated odorants in female mice involves activation of the reward system and basolateral amygdala. The European Journal of Neuroscience 2005, 21(8):2186-2198. 10.1111/j.1460-9568.2005.04036.x.
124. Mucignat-Caretta C., Redaelli M., Caretta A. One nose, one brain: contribution of the main and accessory olfactory system to chemosensation. Frontiers in Neuroanatomy 2012, 6:46. 10.3389/fnana.2012.00046.
125. Munger S.D., Leinders-Zufall T., Zufall F. Subsystem organization of the mammalian sense of smell. Annual Review of Physiology 2009, 71:115-140. 10.1146/annurev.physiol.70.113006.100608.
126. Nishimura K., Utsumi K., Yuhara M., Fujitani Y., Iritani A. Identification of puberty-accelerating pheromones in male mouse urine. The Journal of Experimental Zoology 1989, 251(3):300-305. 10.1002/jez.1402510306.
127. Nodari F., Hsu F.F., Fu X., Holekamp T.F., Kao L.F., Turk J., et al. Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. The Journal of Neuroscience 2008, 28(25):6407-6418. 10.1523/JNEUROSCI.1425-08.2008.
128. Novejarque A., Gutierrez-Castellanos N., Lanuza E., Martinez-Garcia F. Amygdaloid projections to the ventral striatum in mice: direct and indirect chemosensory inputs to the brain reward system. Frontiers in Neuroanatomy 2011, 5:54. 10.3389/fnana.2011.00054.
129. Novotny M. Pheromones, binding proteins and receptor responses in rodents. Biochemical Society Transactions 2003, 31(Pt 1):117-122.
130. Novotny M., Harvey S., Jemiolo B. Chemistry of male dominance in the house mouse, Mus domesticus. Experientia 1990, 46(1):109-113.
131. Novotny M., Harvey S., Jemiolo B., Alberts J. Synthetic pheromones that promote inter-male aggression in mice. Proceedings of the National Academy of Sciences of the United States of America 1985, 82(7):2059-2061.
132. Novotny M., Ma W., Wiesler D., Zidek L. Positive identification of the puberty-accelerating pheromone of the house mouse: the volatile ligands associating with the major urinary protein. Proceedings of the Royal Society B 1999, 266(1432):2017-2022. 10.1098/rspb.1999.0880.
133. Nyby J., Whitney G., Schmitz S., Dizinno G. Postpubertal experience establishes signal value of mammaliam sex odor. Behavioral Biology 1978, 22(4):545-552.
134. Nyby J., Wysocki C.J., Whitney G., Dizinno G., Schneider J. Elicitation of male mouse (Mus musculus) ultrasonic vocalizations: I. Urinary cues. Journal of Comparative and Physiological Psychology 1979, 93(5):957.
135. Papes F., Logan D.W., Stowers L. The vomeronasal organ mediates interspecies defensive behaviors through detection of protein pheromone homologs. Cell 2010, 141(4):692-703. 10.1016/j.cell.2010.03.037.
136. Paredes R.G., Lopez M.E., Baum M.J. Testosterone augments neuronal Fos responses to estrous odors throughout the vomeronasal projection pathway of gonadectomized male and female rats. Hormones and Behavior 1998, 33(1):48-57. 10.1006/hbeh.1998.1435.
137. Pavlov I.P. Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex 1927, Oxford University Press, Oxford, U.K.
138. Peters R.H. Learned aversions to copulatory behaviors in male rats. Behavioral Neuroscience 1983, 97(1):140-145.
139. Pfaus J.G., Kippin T.E., Centeno S. Conditioning and sexual behavior: a review. Hormones and Behavior 2001, 40(2):291-321. 10.1006/hbeh.2001.1686.
140. Pfaus J.G., Kippin T.E., Coria-Avila G.A., Gelez H., Afonso V.M., Ismail N., Parada M. Who, what, where, when (and maybe even why)? How the experience of sexual reward connects sexual desire, preference, and performance. Archives of Sexual Behavior 2012, 41(1):31-62. 10.1007/s10508-012-9935-5.
141. Ponmanickam P., Archunan G., Achiraman S., Sankar R., Saito T., Habara Y. Preputial gland activates olfactory receptor neurons in rat: calcium imaging study using laser scanning confocal microscopy. Indian Journal of Biochemistry and Biophysics 2013, 50(3):242-246.
142. Potegal M. The reinforcing value of several types of aggressive behavior: a review. Aggressive Behavior 1979, 5(4):353-373.
143. Pro-Sistiaga P., Mohedano-Moriano A., Ubeda-Banon I., Del Mar Arroyo-Jimenez M., Marcos P., Artacho-Perula E., et al. Convergence of olfactory and vomeronasal projections in the rat basal telencephalon. The Journal of Comparative Neurology 2007, 504(4):346-362. 10.1002/cne.21455.
144. Rescorla R.A. Behavioral studies of Pavlovian conditioning. Annual Review of Neuroscience 1988, 11:329-352. 10.1146/annurev.ne.11.030188.001553.
145. Riviere S., Challet L., Fluegge D., Spehr M., Rodriguez I. Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors. Nature 2009, 459(7246):574-577. 10.1038/nature08029.
146. Roberts S.A., Davidson A.J., McLean L., Beynon R.J., Hurst J.L. Pheromonal induction of spatial learning in mice. Science 2012, 338(6113):1462-1465. 10.1126/science.1225638.
147. Roberts S.A., Simpson D.M., Armstrong S.D., Davidson A.J., Robertson D.H., McLean L., et al. Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biology 2010, 8:75. 10.1186/1741-7007-8-75.
148. Robinson D.L., Heien M.L., Wightman R.M. Frequency of dopamine concentration transients increases in dorsal and ventral striatum of male rats during introduction of conspecifics. The Journal of Neuroscience 2002, 22(23):10477-10486.
149. Robinson D.L., Phillips P.E., Budygin E.A., Trafton B.J., Garris P.A., Wightman R.M. Sub-second changes in accumbal dopamine during sexual behavior in male rats. Neuroreport 2001, 12(11):2549-2552.
150. Roussel E., Padie S., Giurfa M. Aversive learning overcomes appetitive innate responding in honeybees. Animal Cognition 2012, 15(1):135-141. 10.1007/s10071-011-0426-1.
151. Savic I., Berglund H., Lindstrom P. Brain response to putative pheromones in homosexual men. Proceedings of the National Academy of Sciences of the United States of America 2005, 102(20):7356-7361. 10.1073/pnas.0407998102.
152. Schaal B. Mammary odor cues and pheromones: mammalian infant-directed communication about maternal state, mammae, and milk. Vitamins and Hormones 2010, 83:83-136. 10.1016/S0083-6729(10)83004-3.
153. Schaal B., Coureaud G., Doucet S., Delaunay-El Allam M., Moncomble A.S., Montigny D., et al. Mammary olfactory signalisation in females and odor processing in neonates: ways evolved by rabbits and humans. Behavioural Brain Research 2009, 200(2):346-358.
154. Schaal B., Coureaud G., Langlois D., Ginies C., Semon E., Perrier G. Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 2003, 424(6944):68-72. 10.1038/nature01739.
155. Scott J., Fredericson E. The causes of fighting in mice and rats. Physiological Zoology 1951, 273-309.
156. Skinner B.F. Contingencies of reinforcement: A theoretical analysis 1969, Appleton-Century-Crofts, New York.
157. Sorensen P.W., Christensen T.A., Stacey N.E. Discrimination of pheromonal cues in fish: emerging parallels with insects. Current Opinion in Neurobiology 1998, 8(4):458-467.
158. Spehr M., Kelliher K.R., Li X.H., Boehm T., Leinders-Zufall T., Zufall F. Essential role of the main olfactory system in social recognition of major histocompatibility complex peptide ligands. The Journal of Neuroscience 2006, 26(7):1961-1970. 10.1523/JNEUROSCI.4939-05.2006.
159. Staples L.G., McGregor I.S., Apfelbach R., Hunt G.E. Cat odor, but not trimethylthiazoline (fox odor), activates accessory olfactory and defense-related brain regions in rats. Neuroscience 2008, 151(4):937-947. 10.1016/j.neuroscience.2007.11.039.
160. Stern J.J. Responses of male rats to sex odors. Physiology and Behavior 1970, 5(4):519-524.
161. Stowers L., Holy T.E., Meister M., Dulac C., Koentges G. Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 2002, 295(5559):1493-1500. 10.1126/science.1069259.
162. Stowers L., Logan D.W. Olfactory mechanisms of stereotyped behavior: on the scent of specialized circuits. Current Opinion in Neurobiology 2010, 20(3):274-280. 10.1016/j.conb.2010.02.013.
163. Stowers L., Marton T.F. What is a pheromone? Mammalian pheromonesreconsidered. Neuron 2005, 46(5):699-702. 10.1016/j.neuron.2005.04.032.
164. Sullivan R.M., Landers M., Yeaman B., Wilson D.A. Good memories of bad events in infancy. Nature 2000, 407(6800):38-39. 10.1038/35024156.
165. Swaney W.T., Curley J.P., Champagne F.A., Keverne E.B. Genomic imprinting mediates sexual experience-dependent olfactory learning in male mice. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(14):6084-6089. 10.1073/pnas.0609471104.
166. Swanson L.W. Cerebral hemisphere regulation of motivated behavior. Brain Research 2000, 886(1-2):113-164.
167. Talley H.M., Laukaitis C.M., Karn R.C. Female preference for male saliva: implications for sexual isolation of Mus musculus subspecies. Evolution 2001, 55(3):631-634.
168. Tinbergen N. The study of instinct: With a new introduction 1969, Clarendon Press, Oxford, U.K.
169. Tirindelli R., Dibattista M., Pifferi S., Menini A. From pheromones to behavior. Physiological Reviews 2009, 89(3):921-956. 10.1152/physrev.00037.2008.
170. Vaglio S. Volatile signals during pregnancy. Vitamins and Hormones 2010, 83:289-304. 10.1016/S0083-6729(10)83012-2.
171. Wang L., Anderson D.J. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 2010, 463(7278):227-231. 10.1038/nature08678.
172. Weldon P.J. The evolution of alarm pheromones. Chemical signals in vertebrates 3 1983, 309-312. Springer, New York. D. Muller-Schwarze, R.M. Silverstein (Eds.).
173. White N.M. Reward: what is it? How can it be inferred from behavior?. Neurobiology of sensation and reward 2011, CRC Press, Boca Raton, FL. J.A. Gottfried (Ed.).
174. Wise R.A. Dopamine, learning and motivation. Nature Reviews Neuroscience 2004, 5(6):483-494. 10.1038/nrn1406.
175. Wright N.J. Evolution of the techniques used in studying associative olfactory learning and memory in adult Drosophila invivo: a historical and technical perspective. Invertebrate Neuroscience 2014, 14(1):1-11. 10.1007/s10158-013-0163-z.
176. Wyatt T.D. Pheromones and animal behavior: Chemical signals and signature mixes 2014, Cambridge University Press, Cambridge, U.K.
177. Yuan Q., Harley C.W., McLean J.H. Converging methodologies in a mammalian "simple system" focused on the biology of memory: conditioned odor preference in the neonate rat. Multidisciplinary tools for investigating synaptic plasticity 2013, 223-256. Humana Press Inc., Totowa, NJ. P.V. Ngugen (Ed.).
178. Zahorik D.M., Johnston R.E. Taste aversions to food flavors and vaginal secretion in golden hamsters. Journal of Comparative and Physiological Psychology 1976, 90(1):57-66.
179. Zhang J.X., Sun L., Zhang Y.H. Foxn1 gene knockout suppresses sexual attractiveness and pheromonal components of male urine in inbred mice. Chemical Senses 2010, 35(1):47-56. 10.1093/chemse/bjp081.
180. Zhou W., Chen D. Fear-related chemosignals modulate recognition of fear in ambiguous facial expressions. Psychological Science 2009, 20(2):177-183. 10.1111/j.1467-9280.2009.02263.x.
181. Zhou W., Yang X., Chen K., Cai P., He S., Jiang Y. Chemosensory communication of gender through two human steroids in a sexually dimorphic manner. Current Biology 2014, 24(10):1091-1095. 10.1016/j.cub.2014.03.035.
182. Zufall F., Leinders-Zufall T. Mammalian pheromone sensing. Current Opinion in Neurobiology 2007, 17(4):483-489. 10.1016/j.conb.2007.07.012.