Neural control of sexually dimorphic behaviors

Current Opinion in Neurobiology

Volumn 23, Issue 3, 2013, Pages 330-338

  Manoli, Devanand S ^a   Fan, Pu ^a,b   Fraser, Eleanor J ^a   Shah, Nirao M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AGGRESSION; CONCEPTUAL FRAMEWORK; DROSOPHILA; MATING; MOUSE; NERVE CELL NETWORK; NERVOUS SYSTEM; NONHUMAN; PARENTAL BEHAVIOR; PRIORITY JOURNAL; REPRODUCTION; REVIEW; SEX DIFFERENCE; SEXUAL BEHAVIOR; SEXUALLY DIMORPHIC BEHAVIOR; STEREOTYPY; TISSUE DIFFERENTIATION;

ANIMALS; DROSOPHILA MELANOGASTER; MICE; NERVOUS SYSTEM PHYSIOLOGICAL PROCESSES; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL;

EID: 84878360509     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2013.04.005     Document Type: Review

References (88)

1. Touhara K., Vosshall L.B. Sensing odorants and pheromones with chemosensory receptors. Annu Rev Physiol 2009, 71:307-332.
2. Dulac C., Torello A.T. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 2003, 4:551-562.
3. Roberts S.A., Simpson D.M., Armstrong S.D., Davidson A.J., Robertson D.H., McLean L., Beynon R.J., Hurst J.L. Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male's odour. BMC Biol 2010, 8:75.
4. Nodari F., Hsu F.-F., Fu X., Holekamp T.F., Kao L.-F., Turk J., Holy T.E. Sulfated steroids as natural ligands of mouse pheromone-sensing neurons. J Neurosci 2008, 28:6407-6418.
5. Li Q., Korzan W.J., Ferrero D.M., Chang R.B., Roy D.S., Buchi M., Lemon J.K., Kaur A.W., Stowers L., Fendt M., et al. Synchronous evolution of an odor biosynthesis pathway and behavioral response. Curr Biol 2012, 10.1016/j.cub.2012.10.047.
6. Chamero P., Marton T.F., Logan D.W., Flanagan K., Cruz J.R., Saghatelian A., Cravatt B.F., Stowers L. Identification of protein pheromones that promote aggressive behaviour. Nature 2007, 450:899-902.
7. Kimoto H., Haga S., Sato K., Touhara K. Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 2005, 437:898-901.
8. Kimoto H., Sato K., Nodari F., Haga S., Holy T.E., Touhara K. Sex- and strain-specific expression and vomeronasal activity of mouse ESP family peptides. Curr Biol 2007, 17:1879-1884.
9. Ferveur J.-F. Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 2005, 35:279-295.
10. Wang L., Anderson D.J. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 2010, 463:227-231.
11. Wang L., Han X., Mehren J., Hiroi M., Billeter J.-C., Miyamoto T., Amrein H., Levine J.D., Anderson D.J. Hierarchical chemosensory regulation of male-male social interactions in Drosophila. Nat Neurosci 2011, 14:757-762.
12. Leinders-Zufall T., Brennan P., Widmayer P.S.P.C., Maul-Pavicic A., Jäger M., Li X.-H., Breer H., Zufall F., Boehm T. MHC class I peptides as chemosensory signals in the vomeronasal organ. Science 2004, 306:1033-1037.
13. Van der Goes van Naters W., Carlson J.R. Receptors and neurons for fly odors in Drosophila. Curr Biol 2007, 17:606-612.
14. Isogai Y., Si S., Pont-Lezica L., Tan T., Kapoor V., Murthy V.N., Dulac C. Molecular organization of vomeronasal chemoreception. Nature 2011, 478:241-245.
15. Thistle R., Cameron P., Ghorayshi A., Dennison L., Scott K. Contact chemoreceptors mediate male-male repulsion and male-female attraction during Drosophila courtship. Cell 2012, 149:1140-1151.
16. Toda H., Zhao X., Dickson B.J. The Drosophila female aphrodisiac pheromone activates ppk23(+) sensory neurons to elicit male courtship behavior. Cell Rep 2012, 1:599-607.
17. Lu B., LaMora A., Sun Y., Welsh M.J., Ben-Shahar Y. ppk23-Dependent chemosensory functions contribute to courtship behavior in Drosophila melanogaster. PLoS Genet 2012, 8:e1002587.
18. Haga S., Hattori T., Sato T., Sato K., Matsuda S., Kobayakawa R., Sakano H., Yoshihara Y., Kikusui T., Touhara K. The male mouse pheromone ESP1 enhances female sexual receptive behaviour through a specific vomeronasal receptor. Nature 2010, 466:118-122.
19. Ben-Shaul Y., Katz L.C., Mooney R., Dulac C. In vivo vomeronasal stimulation reveals sensory encoding of conspecific and allospecific cues by the mouse accessory olfactory bulb. Proc Natl Acad Sci U S A 2010, 107:5172-5177.
20. Meeks J.P., Arnson H.A., Holy T.E. Representation and transformation of sensory information in the mouse accessory olfactory system. Nat Neurosci 2010, 13:723-730.
21. Lin D.Y., Zhang S.-Z., Block E., Katz L.C. Encoding social signals in the mouse main olfactory bulb. Nature 2005, 434:470-477.
22. Luo M., Fee M.S., Katz L.C. Encoding pheromonal signals in the accessory olfactory bulb of behaving mice. Science 2003, 299:1196-1201.
23. Ruta V., Datta S.R., Vasconcelos M.L., Freeland J., Looger L.L., Axel R. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 2010, 468:686-690.
24. Datta S.R., Vasconcelos M.L., Ruta V., Luo S., Wong A., Demir E., Flores J., Balonze K., Dickson B.J., Axel R. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 2008, 452:473-477.
25. Marín I., Baker B.S. The evolutionary dynamics of sex determination. Science 1998, 281:1990-1994.
26. Rideout E.J., Dornan A.J., Neville M.C., Eadie S., Goodwin S.F. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat Neurosci 2010, 13:458-466.
27. Robinett C.C., Vaughan A.G., Knapp J.-M., Baker B.S. Sex and the single cell. II. There is a time and place for sex. PLoS Biol 2010, 8:e1000365.
28. Ryner L.C., Goodwin S.F., Castrillon D.H., Anand A., Villella A., Baker B.S., Hall J.C., Taylor B.J., Wasserman S.A. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 1996, 87:1079-1089.
29. Ito H., Fujitani K., Usui K., Shimizu-Nishikawa K., Tanaka S., Yamamoto D Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. Proc Natl Acad Sci U S A 1996, 93:9687-9692.
30. Manoli D.S., Foss M., Villella A., Taylor B.J., Hall J.C., Baker B.S. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 2005, 436:395-400.
31. Stockinger P., Kvitsiani D., Rotkopf S., Tirián L., Dickson B.J. Neural circuitry that governs Drosophila male courtship behavior. Cell 2005, 121:795-807.
32. Demir E., Dickson B.J. fruitless splicing specifies male courtship behavior in Drosophila. Cell 2005, 121:785-794.
33. Villella A., Hall J.C. Courtship anomalies caused by doublesex mutations in Drosophila melanogaster. Genetics 1996, 143:331-344.
34. Mangelsdorf D.J., Thummel C., Beato M., Herrlich P., Schütz G., Umesono K., Blumberg B., Kastner P., Mark M., Chambon P., et al. The nuclear receptor superfamily: the second decade. Cell 1995, 83:835-839.
35. Ryan K.J., Naftolin F., Reddy V., Flores F., Petro Z. Estrogen formation in the brain. Am J Obstet Gynecol 1972, 114:454-460.
36. Morris J.A., Jordan C.L., Breedlove S.M. Sexual differentiation of the vertebrate nervous system. Nat Neurosci 2004, 7:1034-1039.
37. Wu M.V., Manoli D.S., Fraser E.J., Coats J.K., Tollkuhn J., Honda S.-I., Harada N., Shah N.M. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 2009, 139:61-72.
38. Wu M.V., Shah N.M. Control of masculinization of the brain and behavior. Curr Opin Neurobiol 2011, 21:116-123.
39. Juntti S.A., Tollkuhn J., Wu M.V., Fraser E.J., Soderborg T., Tan S., Honda S.-I., Harada N., Shah N.M. The androgen receptor governs the execution, but not programming, of male sexual and territorial behaviors. Neuron 2010, 66:260-272.
40. Raskin K., De Gendt K., Duittoz A., Liere P., Verhoeven G., Tronche F., Mhaouty-Kodja S. Conditional inactivation of androgen receptor gene in the nervous system: effects on male behavioral and neuroendocrine responses. J Neurosci 2009, 29:4461-4470.
41. McCarthy M.M. Estradiol and the developing brain. Physiol Rev 2008, 88:91-124.
42. Bakker J., De Mees C., Douhard Q., Balthazart J., Gabant P., Szpirer J., Szpirer C. Alpha-fetoprotein protects the developing female mouse brain from masculinization and defeminization by estrogens. Nat Neurosci 2006, 9:220-226.
43. Xu X., Coats J.K., Yang C.F., Wang A., Ahmed O.M., Alvarado M., Izumi T., Shah N.M. Modular genetic control of sexually dimorphic behaviors. Cell 2012, 148:596-607.
44. Bray S., Amrein H. A putative Drosophila pheromone receptor expressed in male-specific taste neurons is required for efficient courtship. Neuron 2003, 39:1019-1029.
45. Watanabe K., Toba G., Koganezawa M., Yamamoto D. Gr39a, a highly diversified gustatory receptor in Drosophila, has a role in sexual behavior. Behav Genet 2011, 41:746-753.
46. Kurtovic A., Widmer A., Dickson B.J. A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 2007, 446:542-546.
47. Moon S.J., Lee Y., Jiao Y., Montell C. A Drosophila gustatory receptor essential for aversive taste and inhibiting male-to-male courtship. Curr Biol 2009, 19:1623-1627.
48. Miyamoto T., Amrein H. Suppression of male courtship by a Drosophila pheromone receptor. Nat Neurosci 2008, 11:874-876.
49. Mellert D.J., Knapp J.-M., Manoli D.S., Meissner G.W., Baker B.S. Midline crossing by gustatory receptor neuron axons is regulated by fruitless, doublesex and the Roundabout receptors. Development 2010, 137:323-332.
50. Ejima A., Smith B.P.C., Lucas C., Van der Goes van Naters W., Miller C.J., Carlson J.R., Levine J.D., Griffith L.C. Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate. Curr Biol 2007, 17:599-605.
51. Liu W., Liang X., Gong J., Yang Z., Zhang Y.-H., Zhang J.-X., Rao Y. Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat Neurosci 2011, 14:896-902.
52. Mandiyan V.S., Coats J.K., Shah N.M. Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat Neurosci 2005, 8:1660-1662.
53. 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. Proc Natl Acad Sci U S A 2002, 99:6376-6381.
54. 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, 295:1493-1500.
55. Yoon H., Enquist L.W., Dulac C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 2005, 123:669-682.
56. Kimchi T., Xu J., Dulac C. A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 2007, 448:1009-1014.
57. Edwards D.A., Burge K.G. Early androgen treatment and male and female sexual behavior in mice. Horm Behav 1971, 2:49-58.
58. Roberts S.A., Davidson A.J., McLean L., Beynon R.J., Hurst J.L. Pheromonal induction of spatial learning in mice. Science 2012, 338:1462-1465.
59. Cachero S., Ostrovsky A.D., Yu J.Y., Dickson B.J., Jefferis G.S.X.E. Sexual dimorphism in the fly brain. Curr Biol 2010, 20:1589-1601.
60. Yu J.Y., Kanai M.I., Demir E., Jefferis G.S.X.E., Dickson B.J. Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 2010, 20:1602-1614.
61. Kohatsu S., Koganezawa M., Yamamoto D. Female contact activates male-specific interneurons that trigger stereotypic courtship behavior in Drosophila. Neuron 2011, 69:498-508.
62. Von Philipsborn A.C., Liu T., Yu J.Y., Masser C., Bidaye S.S., Dickson B.J. Neuronal control of Drosophila courtship song. Neuron 2011, 69:509-522.
63. Pan Y., Meissner G.W., Baker B.S. Joint control of Drosophila male courtship behavior by motion cues and activation of male-specific P1 neurons. Proc Natl Acad Sci U S A 2012, 109:10065-10070.
64. Ito H., Sato K., Koganezawa M., Ote M., Matsumoto K., Hama C., Yamamoto D. Fruitless recruits two antagonistic chromatin factors to establish single-neuron sexual dimorphism. Cell 2012, 149:1327-1338.
65. Lin D., Boyle M.P., Dollar P., Lee H., Lein E.S., Perona P., Anderson D.J. Functional identification of an aggression locus in the mouse hypothalamus. Nature 2011, 470:221-226.
66. Hess W.R., Akert K. Experimental data on role of hypothalamus in mechanism of emotional behavior. AMA Arch Neurol Psychiatry 1955, 73:127-129.
67. Bard P. A diencephalic mechanism for the expression of rage with special reference to the sympathetic nervous system. Am J Physiol 1928, 84:490-515.
68. Kruk M.R., Van der Poel A.M., De Vos-Frerichs T.P. The induction of aggressive behaviour by electrical stimulation in the hypothalamus of male rats. Behaviour 1979, 70:292-322.
69. Olivier B., Wiepkema P.R. Behaviour changes in mice following electrolytic lesions in the median hypothalamus. Brain Res 1974, 65:521-524.
70. Musatov S., Chen W., Pfaff D.W., Kaplitt M.G., Ogawa S. RNAi-mediated silencing of estrogen receptor in the ventromedial nucleus of hypothalamus abolishes female sexual behaviors. Proc Natl Acad Sci U S A 2006, 103:10456-10460.
71. Musatov S., Chen W., Pfaff D.W., Mobbs C.V., Yang X.-J., Clegg D.J., Kaplitt M.G., Ogawa S Silencing of estrogen receptor alpha in the ventromedial nucleus of hypothalamus leads to metabolic syndrome. Proc Natl Acad Sci U S A 2007, 104:2501-2506.
72. De Vries G.J. Sex differences in neurotransmitter systems. J Neuroendocrinol 1990, 2:1-13.
73. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 2002, 25:507-536.
74. Arnold A.P., Chen X. What does the "four core genotypes" mouse model tell us about sex differences in the brain and other tissues?. Front Neuroendocrinol 2009, 30:1-9.
75. De Vries G.J., Rissman E.F., Simerly R.B., Yang L.-Y., Scordalakes E.M., Auger C.J., Swain A., Lovell-Badge R., Burgoyne P.S., Arnold A.P. A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J Neurosci 2002, 22:9005-9014.
76. Gregg C., Zhang J., Butler J.E., Haig D., Dulac C. Sex-specific parent-of-origin allelic expression in the mouse brain. Science 2010, 329:682-685.
77. Gregg C., Zhang J., Weissbourd B., Luo S., Schroth G.P., Haig D., Dulac C. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 2010, 329:643-648.
78. DeVeale B., Van der Kooy D., Babak T. Critical evaluation of imprinted gene expression by RNA-Seq: a new perspective. PLoS Genet 2012, 8:e1002600.
79. Lefebvre L., Viville S., Barton S.C., Ishino F., Keverne E.B., Surani M.A. Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nat Genet 1998, 20:163-169.
80. Garfield A.S., Cowley M., Smith F.M., Moorwood K., Stewart-Cox J.E., Gilroy K., Baker S., Xia J., Dalley J.W., Hurst L.D., et al. Distinct physiological and behavioural functions for parental alleles of imprinted Grb10. Nature 2011, 469:534-538.
81. Liu Y., Jiang Y., Si Y., Kim J.-Y., Chen Z.-F., Rao Y. Molecular regulation of sexual preference revealed by genetic studies of 5-HT in the brains of male mice. Nature 2011, 472:95-99.
82. Shohat-Ophir G., Kaun K.R., Azanchi R., Mohammed H., Heberlein U. Sexual deprivation increases ethanol intake in Drosophila. Science 2012, 335:1351-1355.
83. Kim W.J., Jan L.Y., Jan Y.N. Contribution of visual and circadian neural circuits to memory for prolonged mating induced by rivals. Nat Neurosci 2012, 15:876-883.
84. Grosjean Y., Rytz R., Farine J.-P., Abuin L., Cortot J., Jefferis G.S.X.E., Benton R. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 2011, 478:236-240.
85. Keleman K., Vrontou E., Krüttner S., Yu J.Y., Kurtovic-Kozaric A., Dickson B.J. Dopamine neurons modulate pheromone responses in Drosophila courtship learning. Nature 2012, 489:145-149.
86. Wang L., Dankert H., Perona P., Anderson D.J. A common genetic target for environmental and heritable influences on aggressiveness in Drosophila. Proc Natl Acad Sci U S A 2008, 105:5657-5663.
87. Certel S.J., Leung A., Lin C.-Y., Perez P., Chiang A.-S., Kravitz E.A. Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males. PLoS ONE 2010, 5:e13248.
88. Zhou C., Huang H., Kim S.M., Lin H., Meng X., Han K.-A., Chiang A.-S., Wang J.W., Jiao R., Rao Y. Molecular genetic analysis of sexual rejection: roles of octopamine and its receptor OAMB in Drosophila courtship conditioning. J Neurosci 2012, 32:14281-14287.