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A neurogenetic mechanism of experience-dependent suppression of aggression

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Ishii, Kenichi, Cortese, Matteo, Leng, Xubo, Shokhirev, Maxim N., Asahina, Kenta·2022·Science Advances

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Abstract

Aggression is an ethologically important social behavior, but excessive aggression can be detrimental to fitness. Social experiences among conspecific individuals reduce aggression in many species, the mechanism of which is largely unknown. We found that loss-of-function mutation of nervy ( nvy ), a Drosophila homolog of vertebrate myeloid translocation genes (MTGs), increased aggressiveness only in socially experienced flies and that this could be reversed by neuronal expression of human MTGs. A subpopulation of octopaminergic/tyraminergic neurons labeled by nvy was specifically required for such social experience–dependent suppression of aggression, in both males and females. Cell type–specific transcriptomic analysis of these neurons revealed aggression-controlling genes that are likely downstream of nvy . Our results illustrate both genetic and neuronal mechanisms by which the nervous system suppresses aggression in a social experience–dependent manner, a poorly understood process that is considered important for maintaining the fitness of animals.

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  1. [1]J. M. Smith, Evolution and the Theory of Games (Cambridge Univ. Press, 1982).
  2. [2]H. A. Dierick, R. J. Greenspan, Molecular analysis of flies selected for aggressive behavior. Nat. Genet. 38, 1023– 1031 (2006). 16906161
  3. [3]J. Shorter, C. Couch, W. Huang, M. A. Carbone, J. Peiffer, R. R. H. Anholt, T. F. C. Mackay, Genetic architecture of natural variation in Drosophila melanogaster aggressive behavior. Proc. Natl. Acad. Sci. U.S.A. 112, E3555– E3563 (2015). 26100892 PMC4500262
  4. [4]S. A. Golden, M. Heshmati, M. Flanigan, D. J. Christoffel, K. Guise, M. L. Pfau, H. Aleyasin, C. Menard, H. Zhang, G. E. Hodes, D. Bregman, L. Khibnik, J. Tai, N. Rebusi, B. Krawitz, D. Chaudhury, J. J. Walsh, M.-H. Han, M. L. Shapiro, S. J. Russo, Basal forebrain projections to the lateral habenula modulate aggression reward. Nature 534, 688– 692 (2016). 27357796 PMC4930107
  5. [5]M. Briffa, L. U. Sneddon, A. J. Wilson, Animal personality as a cause and consequence of contest behaviour. Biol. Lett. 11, 20141007 (2015). 25808004 PMC4387495
  6. [6]Y. Hsu, R. L. Earley, L. L. Wolf, Modulation of aggressive behaviour by fighting experience: Mechanisms and contest outcomes. Biol. Rev. Camb. Philos. Soc. 81, 33– 74 (2006). 16460581
  7. [7]L. Wang, H. Dankert, P. Perona, D. J. Anderson, A common genetic target for environmental and heritable influences on aggressiveness in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 105, 5657– 5663 (2008). 18408154 PMC2311352
  8. [8]J. K. Penn, M. F. Zito, E. A. Kravitz, A single social defeat reduces aggression in a highly aggressive strain of Drosophila. Proc. Natl. Acad. Sci. U.S.A. 107, 12682– 12686 (2010). 20616023 PMC2906583
  9. [11]V. Diaz, D. Lin, Neural circuits for coping with social defeat. Curr. Opin. Neurobiol. 60, 99– 107 (2020). 31837481 PMC7002193
  10. [12]D. An, W. Chen, D.-Q. Yu, S.-W. Wang, W.-Z. Yu, H. Xu, D.-M. Wang, D. Zhao, Y.-P. Sun, J.-C. Wu, Y.-Y. Tang, S.-M. Yin, Effects of social isolation, re-socialization and age on cognitive and aggressive behaviors of Kunming mice and BALB/c mice. Anim. Sci. J. 88, 798– 806 (2017). 27619417
  11. [13]K. J. Flannelly, R. J. Blanchard, M. Y. Muraoka, L. Flannelly, Copulation increases offensive attack in male rats. Physiol. Behav. 29, 381– 385 (1982). 6890693
  12. [14]Q. Yuan, Y. Song, C.-H. Yang, L. Y. Jan, Y. N. Jan, Female contact modulates male aggression via a sexually dimorphic GABAergic circuit in Drosophila. Nat. Neurosci. 17, 81– 88 (2014). 24241395 PMC3995170
  13. [16]J. B. Saltz, Genetic variation in social environment construction influences the development of aggressive behavior in Drosophila melanogaster. Heredity (Edinb) 118, 340– 347 (2017). 27848947 PMC5345599
  14. [17]R. J. Kilgour, A. G. McAdam, G. S. Betini, D. R. Norris, Experimental evidence that density mediates negative frequency-dependent selection on aggression. J. Anim. Ecol. 87, 1091– 1101 (2018). 29446094
  15. [18]P. Ramdya, J. Schneider, J. D. Levine, The neurogenetics of group behavior in Drosophila melanogaster. J. Exp. Biol. 220, 35– 41 (2017). 28057826
  16. [21]K. Asahina, Neuromodulation and strategic action choice in Drosophila aggression. Annu. Rev. Neurosci. 40, 51– 75 (2017). 28375770
  17. [22]E. D. Hoopfer, Neural control of aggression in Drosophila. Curr. Opin. Neurobiol. 38, 109– 118 (2016). 27179788
  18. [23]J. E. Lischinsky, D. Lin, Neural mechanisms of aggression across species. Nat. Neurosci. 23, 1317– 1328 (2020). 33046890 PMC13152643
  19. [24]P. Chen, W. Hong, Neural circuit mechanisms of social behavior. Neuron 98, 16– 30 (2018). 29621486 PMC6028944
  20. [26]M.-Y. Chou, R. Amo, M. Kinoshita, B.-W. Cherng, H. Shimazaki, M. Agetsuma, T. Shiraki, T. Aoki, M. Takahoko, M. Yamazaki, S. Higashijima, H. Okamoto, Social conflict resolution regulated by two dorsal habenular subregions in zebrafish. Science 352, 87– 90 (2016). 27034372
  21. [27]J. Rillich, P. A. Stevenson, A fighter’s comeback: Dopamine is necessary for recovery of aggression after social defeat in crickets. Horm. Behav. 66, 696– 704 (2014). 25268421
  22. [28]A. C. Nelson, V. Kapoor, E. Vaughn, J. A. Gnanasegaram, N. D. Rubinstein, V. N. Murthy, C. Dulac, Molecular and circuit architecture of social hierarchy. bioRxiv 838664 (2019). PMC12458795 40795854
  23. [29]H. A. Dierick, R. J. Greenspan, Serotonin and neuropeptide F have opposite modulatory effects on fly aggression. Nat. Genet. 39, 678– 682 (2007). 17450142
  24. [30]O. Cases, I. Seif, J. Grimsby, P. Gaspar, K. Chen, S. Pournin, U. Muller, M. Aguet, C. Babinet, J. C. Shih, E. De Maeyer, Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268, 1763– 1766 (1995). 7792602 PMC2844866
  25. [31]Z. Wu, A. E. Autry, J. F. Bergan, M. Watabe-Uchida, C. G. Dulac, Galanin neurons in the medial preoptic area govern parental behaviour. Nature 509, 325– 330 (2014). 24828191 PMC4105201
  26. [32]M. S. Kayser, B. Mainwaring, Z. Yue, A. Sehgal, Sleep deprivation suppresses aggression in Drosophila. eLife 4, e07643 (2015). 26216041 PMC4515473
  27. [33]W. Liu, X. Liang, J. Gong, Z. Yang, Y.-H. Zhang, J.-X. Zhang, Y. Rao, Social regulation of aggression by pheromonal activation of Or65a olfactory neurons in Drosophila. Nat. Neurosci. 14, 896– 902 (2011). 21685916
  28. [34]M. Ramin, C. Domocos, D. Slawaska-Eng, Y. Rao, Aggression and social experience: Genetic analysis of visual circuit activity in the control of aggressiveness in Drosophila. Mol. Brain 7, 55 (2014). 25116850 PMC4237967
  29. [35]J. M. Donlea, N. Ramanan, P. J. Shaw, Use-dependent plasticity in clock neurons regulates sleep need in Drosophila. Science 324, 105– 108 (2009). 19342592 PMC2850598
  30. [36]M. Eddison, A genetic screen for Drosophila social isolation mutants and analysis of sex pistol. Sci. Rep. 11, 17395 (2021). 34462500 PMC8405609
  31. [37]P. Agrawal, D. Kao, P. Chung, L. L. Looger, The neuropeptide Drosulfakinin regulates social isolation-induced aggression in Drosophila. J. Exp. Biol. 223, jeb207407 (2020). 31900346 PMC7033730
  32. [38]W. Li, Z. Wang, S. Syed, C. Lyu, S. Lincoln, J. O’Neil, A. D. Nguyen, I. Feng, M. W. Young, Chronic social isolation signals starvation and reduces sleep in Drosophila. Nature 597, 239– 244 (2021). 34408325 PMC8429171
  33. [39]M. Eddison, D. J. Guarnieri, L. Cheng, C.-H. Liu, K. G. Moffat, G. Davis, U. Heberlein, arouser reveals a role for synapse number in the regulation of ethanol sensitivity. Neuron 70, 979– 990 (2011). 21658589
  34. [40]S. C. Hoyer, A. Eckart, A. Herrel, T. Zars, S. A. Fischer, S. L. Hardie, M. Heisenberg, Octopamine in male aggression of Drosophila. Curr. Biol. 18, 159– 167 (2008). 18249112
  35. [41]C. Zhou, Y. Rao, Y. Rao, A subset of octopaminergic neurons are important for Drosophila aggression. Nat. Neurosci. 11, 1059– 1067 (2008). 19160504
  36. [42]K. Watanabe, H. Chiu, B. D. Pfeiffer, A. M. Wong, E. D. Hoopfer, G. M. Rubin, D. J. Anderson, A circuit node that integrates convergent input from neuromodulatory and social behavior-promoting neurons to control aggression in Drosophila. Neuron 95, 1112, 1128.e7 (2017). 28858617 PMC5588916
  37. [43]L. M. Sherer, E. Catudio Garrett, H. R. Morgan, E. D. Brewer, L. A. Sirrs, H. K. Shearin, J. L. Williams, B. D. McCabe, R. S. Stowers, S. J. Certel, Octopamine neuron dependent aggression requires dVGLUT from dual-transmitting neurons. PLOS Genet. 16, e1008609 (2020). 32097408 PMC7059954
  38. [44]J. C. Andrews, M. P. Fernandez, Q. Yu, G. P. Leary, A. K. Leung, M. P. Kavanaugh, E. A. Kravitz, S. J. Certel, Octopamine neuromodulation regulates Gr32a-linked aggression and courtship pathways in Drosophila males. PLOS Genet. 10, e1004356 (2014). 24852170 PMC4031044
  39. [46]X. Leng, M. Wohl, K. Ishii, P. Nayak, K. Asahina, Quantifying influence of human choice on the automated detection of Drosophila behavior by a supervised machine learning algorithm. PLOS ONE 15, e0241696 (2020). 33326445 PMC7743940
  40. [47]M. A. Dow, F. von Schilcher, Aggression and mating success in Drosophila melanogaster. Nature 254, 511– 512 (1975). 804664
  41. [48]S. Chen, A. Y. Lee, N. M. Bowens, R. Huber, E. A. Kravitz, Fighting fruit flies: A model system for the study of aggression. Proc. Natl. Acad. Sci. U.S.A. 99, 5664– 5668 (2002). 11960020 PMC122828
  42. [49]H. Chiu, E. D. Hoopfer, M. L. Coughlan, H. J. Pavlou, S. F. Goodwin, D. J. Anderson, A circuit logic for sexually shared and dimorphic aggressive behaviors in Drosophila. Cell 184, 507– 520.e16 (2021). 33382967 PMC7856078
  43. [50]J. C. Hall, The mating of a fly. Science 264, 1702– 1714 (1994). 8209251
  44. [51]D. Yamamoto, M. Koganezawa, Genes and circuits of courtship behaviour in Drosophila males. Nat. Rev. Neurosci. 14, 681– 692 (2013). 24052176
  45. [52]A. J. Calhoun, J. W. Pillow, M. Murthy, Unsupervised identification of the internal states that shape natural behavior. Nat. Neurosci. 22, 2040– 2049 (2019). 31768056 PMC7819718
  46. [53]J. C. Hall, Courtship among males due to a male-sterile mutation in Drosophila melanogaster. Behav. Genet. 8, 125– 141 (1978). 99136
  47. [54]R. Thistle, P. Cameron, A. Ghorayshi, L. Dennison, K. Scott, Contact chemoreceptors mediate male-male repulsion and male-female attraction during Drosophila courtship. Cell 149, 1140– 1151 (2012). 22632976 PMC3365544
  48. [55]N. Svetec, J.-F. Ferveur, Social experience and pheromonal perception can change male-male interactions in Drosophila melanogaster. J. Exp. Biol. 208, 891– 898 (2005). 15755887
  49. [56]E. Eyjolfsdottir, S. Branson, X. P. Burgos-Artizzu, E. D. Hoopfer, J. Schor, D. J. Anderson, P. Perona, Detecting social actions of fruit flies. Computer Vision – ECCV 8690, 772– 787 (2014).
  50. [58]I. M. A. Ribeiro, M. Drews, A. Bahl, C. Machacek, A. Borst, B. J. Dickson, Visual projection neurons mediating directed courtship in Drosophila. Cell 174, 607– 621.e18 (2018). 30033367
  51. [59]S. Kohatsu, D. Yamamoto, Visually induced initiation of Drosophila innate courtship-like following pursuit is mediated by central excitatory state. Nat. Commun. 6, 6457 (2015). 25743851
  52. [60]S. P. Nilsen, Y.-B. Chan, R. Huber, E. A. Kravitz, Gender-selective patterns of aggressive behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 101, 12342– 12347 (2004). 15302936 PMC514477
  53. [61]L. Wang, D. J. Anderson, Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463, 227– 231 (2010). 19966787 PMC2999963
  54. [62]A. Kurtovic, A. Widmer, B. J. Dickson, A single class of olfactory neurons mediates behavioural responses to a Drosophila sex pheromone. Nature 446, 542– 546 (2007). 17392786
  55. [63]H.-H. Lin, D.-S. Cao, S. Sethi, Z. Zeng, J. S. R. Chin, T. S. Chakraborty, A. K. Shepherd, C. A. Nguyen, J. Y. Yew, C.-Y. Su, J. W. Wang, Hormonal modulation of pheromone detection enhances male courtship success. Neuron 90, 1272– 1285 (2016). 27263969 PMC4911275
  56. [64]S. H. Cole, G. E. Carney, C. A. McClung, S. S. Willard, B. J. Taylor, J. Hirsh, Two functional but noncomplementing Drosophila tyrosine decarboxylase genes: Distinct roles for neural tyramine and octopamine in female fertility. J. Biol. Chem. 280, 14948– 14955 (2005). 15691831
  57. [65]S. Busch, M. Selcho, K. Ito, H. Tanimoto, A map of octopaminergic neurons in the Drosophila brain. J. Comp. Neurol. 513, 643– 667 (2009). 19235225
  58. [66]J. Wildonger, R. S. Mann, Evidence that nervy, the Drosophila homolog of ETO/MTG8, promotes mechanosensory organ development by enhancing Notch signaling. Dev. Biol. 286, 507– 520 (2005). 16168983
  59. [67]M. Selcho, D. Pauls, B. El Jundi, R. F. Stocker, A. S. Thum, The role of octopamine and tyramine in Drosophila larval locomotion. J. Comp. Neurol. 520, 3764– 3785 (2012). 22627970
  60. [68]M. E. Flanigan, H. Aleyasin, L. Li, C. J. Burnett, K. L. Chan, K. B. LeClair, E. K. Lucas, B. Matikainen-Ankney, R. Durand-de Cuttoli, A. Takahashi, C. Menard, M. L. Pfau, S. A. Golden, S. Bouchard, E. S. Calipari, E. J. Nestler, R. J. DiLeone, A. Yamanaka, G. W. Huntley, R. L. Clem, S. J. Russo, Orexin signaling in GABAergic lateral habenula neurons modulates aggressive behavior in male mice. Nat. Neurosci. 23, 638– 650 (2020). 32284606 PMC7195257
  61. [70]S. J. Certel, A. Leung, C.-Y. Lin, P. Perez, A.-S. Chiang, E. A. Kravitz, Octopamine neuromodulatory effects on a social behavior decision-making network in Drosophila males. PLOS ONE 5, e13248 (2010). 20967276 PMC2953509
  62. [71]M. Koganezawa, K. Kimura, D. Yamamoto, The neural circuitry that functions as a switch for courtship versus aggression in Drosophila males. Curr. Biol. 26, 1395– 1403 (2016). 27185554
  63. [72]H. Lee, D.-W. Kim, R. Remedios, T. E. Anthony, A. Chang, L. Madisen, H. Zeng, D. J. Anderson, Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus. Nature 509, 627– 632 (2014). 24739975 PMC4098836
  64. [73]K. Hashikawa, Y. Hashikawa, R. Tremblay, J. Zhang, J. E. Feng, A. Sabol, W. T. Piper, H. Lee, B. Rudy, D. Lin, Esr1+ cells in the ventromedial hypothalamus control female aggression. Nat. Neurosci. 20, 1580– 1590 (2017). 28920934 PMC5953764
  65. [75]J. Wang, T. Hoshino, R. L. Redner, S. Kajigaya, J. M. Liu, ETO, fusion partner in t(8;21) acute myeloid leukemia, represses transcription by interaction with the human N-CoR/mSin3/HDAC1 complex. Proc. Natl. Acad. Sci. U.S.A. 95, 10860– 10865 (1998). 9724795 PMC27986
  66. [76]B. Lutterbach, J. J. Westendorf, B. Linggi, A. Patten, M. Moniwa, J. R. Davie, K. D. Huynh, V. J. Bardwell, R. M. Lavinsky, M. G. Rosenfeld, C. Glass, E. Seto, S. W. Hiebert, ETO, a target of t(8;21) in acute leukemia, interacts with the N-CoR and mSin3 corepressors. Mol. Cell. Biol. 18, 7176– 7184 (1998). 9819404 PMC109299
  67. [78]J. Wildonger, R. S. Mann, The t(8;21) translocation converts AML1 into a constitutive transcriptional repressor. Development 132, 2263– 2272 (2005). 15829516
  68. [79]J. N. Davis, L. McGhee, S. Meyers, The ETO (MTG8) gene family. Gene 303, 1– 10 (2003). 12559562
  69. [80]J. Zhang, B. A. Hug, E. Y. Huang, C. W. Chen, V. Gelmetti, M. Maccarana, S. Minucci, P. G. Pelicci, M. A. Lazar, Oligomerization of ETO is obligatory for corepressor interaction. Mol. Cell. Biol. 21, 156– 163 (2001). 11113190 PMC88789
  70. [81]Y. Liu, M. D. Cheney, J. J. Gaudet, M. Chruszcz, S. M. Lukasik, D. Sugiyama, J. Lary, J. Cole, Z. Dauter, W. Minor, N. A. Speck, J. H. Bushweller, The tetramer structure of the Nervy homology two domain, NHR2, is critical for AML1/ETO’s activity. Cancer Cell 9, 249– 260 (2006). 16616331
  71. [82]B. Tasic, Z. Yao, L. T. Graybuck, K. A. Smith, T. N. Nguyen, D. Bertagnolli, J. Goldy, E. Garren, M. N. Economo, S. Viswanathan, O. Penn, T. Bakken, V. Menon, J. Miller, O. Fong, K. E. Hirokawa, K. Lathia, C. Rimorin, M. Tieu, R. Larsen, T. Casper, E. Barkan, M. Kroll, S. Parry, N. V. Shapovalova, D. Hirschstein, J. Pendergraft, H. A. Sullivan, T. K. Kim, A. Szafer, N. Dee, P. Groblewski, I. Wickersham, A. Cetin, J. A. Harris, B. P. Levi, S. M. Sunkin, L. Madisen, T. L. Daigle, L. Looger, A. Bernard, J. Phillips, E. Lein, M. Hawrylycz, K. Svoboda, A. R. Jones, C. Koch, H. Zeng, Shared and distinct transcriptomic cell types across neocortical areas. Nature 563, 72– 78 (2018). 30382198 PMC6456269
  72. [84]F. Wu, B. Deng, N. Xiao, T. Wang, Y. Li, R. Wang, K. Shi, D.-G. Luo, Y. Rao, C. Zhou, A neuropeptide regulates fighting behavior in Drosophila melanogaster. eLife 9, e54229 (2020). 32314736 PMC7173970
  73. [85]S. M. Davis, A. L. Thomas, K. J. Nomie, L. Huang, H. A. Dierick, Tailless and atrophin control Drosophila aggression by regulating neuropeptide signalling in the pars intercerebralis. Nat. Commun. 5, 3177 (2014). 24495972
  74. [86]B. A. Hug, M. A. Lazar, ETO interacting proteins. Oncogene 23, 4270– 4274 (2004). 15156183
  75. [87]M. A. Fischer, I. Moreno-Miralles, A. Hunt, B. J. Chyla, S. W. Hiebert, Myeloid translocation gene 16 is required for maintenance of haematopoietic stem cell quiescence. EMBO J. 31, 1494– 1505 (2012). 22266796 PMC3321173
  76. [88]J. R. Terman, A. L. Kolodkin, Nervy links protein kinase a to plexin-mediated semaphorin repulsion. Science 303, 1204– 1207 (2004). 14976319
  77. [89]R. J. Ice, J. Wildonger, R. S. Mann, S. W. Hiebert, Comment on “Nervy links protein kinase a to plexin-mediated semaphorin repulsion”. Science 309, 558 (2005). 16040690
  78. [90]J. R. Terman, A. L. Kolodkin, Response to comment on “Nervy links protein kinase a to plexin-mediated semaphorin repulsion”. Science 309, 558 (2005). 16040690
  79. [91]C. E. Holt, K. C. Martin, E. M. Schuman, Local translation in neurons: Visualization and function. Nat. Struct. Mol. Biol. 26, 557– 566 (2019). 31270476
  80. [92]N. Koyano-Nakagawa, C. Kintner, The expression and function of MTG/ETO family proteins during neurogenesis. Dev. Biol. 278, 22– 34 (2005). 15649458
  81. [93]K. Yoon, N. Gaiano, Notch signaling in the mammalian central nervous system: Insights from mouse mutants. Nat. Neurosci. 8, 709– 715 (2005). 15917835
  82. [94]N. C. Inestrosa, E. Arenas, Emerging roles of Wnts in the adult nervous system. Nat. Rev. Neurosci. 11, 77– 86 (2010). 20010950
  83. [96]H. Youn, C. Kirkhart, J. Chia, K. Scott, A subset of octopaminergic neurons that promotes feeding initiation in Drosophila melanogaster. PLOS ONE 13, e0198362 (2018). 29949586 PMC6021039
  84. [97]S. Sayin, J.-F. De Backer, K. P. Siju, M. E. Wosniack, L. P. Lewis, L.-M. Frisch, B. Gansen, P. Schlegel, A. Edmondson-Stait, N. Sharifi, C. B. Fisher, S. A. Calle-Schuler, J. S. Lauritzen, D. D. Bock, M. Costa, G. S. X. E. Jefferis, J. Gjorgjieva, I. C. Grunwald Kadow, A neural circuit arbitrates between persistence and withdrawal in hungry Drosophila. Neuron 104, 544– 558.e6 (2019). 31471123 PMC6839618
  85. [98]Y. Aso, D. Hattori, Y. Yu, R. M. Johnston, N. A. Iyer, T.-T. Ngo, H. Dionne, L. F. Abbott, R. Axel, H. Tanimoto, G. M. Rubin, The neuronal architecture of the mushroom body provides a logic for associative learning. eLife 3, e04577 (2014). 25535793 PMC4273437
  86. [99]F. Li, J. W. Lindsey, E. C. Marin, N. Otto, M. Dreher, G. Dempsey, I. Stark, A. S. Bates, M. W. Pleijzier, P. Schlegel, A. Nern, S. Takemura, N. Eckstein, T. Yang, A. Francis, A. Braun, R. Parekh, M. Costa, L. K. Scheffer, Y. Aso, G. S. Jefferis, L. F. Abbott, A. Litwin-Kumar, S. Waddell, G. M. Rubin, The connectome of the adult Drosophila mushroom body provides insights into function. eLife 9, e62576 (2020). 33315010 PMC7909955
  87. [100]A. Crocker, M. Shahidullah, I. B. Levitan, A. Sehgal, Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 65, 670– 681 (2010). 20223202 PMC2862355
  88. [101]E. E. LeDue, K. Mann, E. Koch, B. Chu, R. Dakin, M. D. Gordon, Starvation-induced depotentiation of bitter taste in Drosophila. Curr. Biol. 26, 2854– 2861 (2016). 27720624
  89. [103]A. C. Groth, M. Fish, R. Nusse, M. P. Calos, Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166, 1775– 1782 (2004). 15126397 PMC1470814
  90. [104]B. D. Pfeiffer, T.-T. Ngo, K. L. Hibbard, C. Murphy, A. Jenett, J. W. Truman, G. M. Rubin, Refinement of tools for targeted gene expression in Drosophila. Genetics 186, 735– 755 (2010). 20697123 PMC2942869
  91. [105]S. J. Gratz, F. P. Ukken, C. D. Rubinstein, G. Thiede, L. K. Donohue, A. M. Cummings, K. M. O’Connor-Giles, Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics 196, 961– 971 (2014). 24478335 PMC3982687
  92. [106]A. Thomas, P.-J. Lee, J. E. Dalton, K. J. Nomie, L. Stoica, M. Costa-Mattioli, P. Chang, S. Nuzhdin, M. N. Arbeitman, H. A. Dierick, A versatile method for cell-specific profiling of translated mRNAs in Drosophila. PLOS ONE 7, e40276 (2012). 22792260 PMC3391276
  93. [107]S.-J. Lee, H. Xu, C. Montell, Rhodopsin kinase activity modulates the amplitude of the visual response in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 101, 11874– 11879 (2004). 15289614 PMC511067
  94. [108]T. Hummel, M. L. Vasconcelos, J. C. Clemens, Y. Fishilevich, L. B. Vosshall, S. L. Zipursky, Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37, 221– 231 (2003). 12546818
  95. [110]K. Asahina, K. Watanabe, B. J. Duistermars, E. Hoopfer, C. R. Gonzalez, E. A. Eyjolfsdottir, P. Perona, D. J. Anderson, Tachykinin-expressing neurons control male-specific aggressive arousal in Drosophila. Cell 156, 221– 235 (2014). 24439378 PMC3978814
  96. [111]H. K. Inagaki, Y. Jung, E. D. Hoopfer, A. M. Wong, N. Mishra, J. Y. Lin, R. Y. Tsien, D. J. Anderson, Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nat. Methods 11, 325– 332 (2014). 24363022 PMC4151318
  97. [112]K. Ishii, M. Wohl, A. DeSouza, K. Asahina, Sex-determining genes distinctly regulate courtship capability and target preference via sexually dimorphic neurons. eLife 9, e52701 (2020). 32314964 PMC7173972
  98. [113]K. Keleman, S. Kruttner, M. Alenius, B. J. Dickson, Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat. Neurosci. 10, 1587– 1593 (2007). 17965711
  99. [114]A. A. Robie, A. D. Straw, M. H. Dickinson, Object preference by walking fruit flies, Drosophila melanogaster, is mediated by vision and graviperception. J. Exp. Biol. 213, 2494– 2506 (2010). 20581279 PMC2892423
  100. [115]S. Agrawal, M. H. Dickinson, The effects of target contrast on Drosophila courtship. J. Exp. Biol. 222, jeb203414 (2019). 31315932
  101. [116]Y. Pan, G. W. Meissner, B. S. Baker, Joint control of Drosophila male courtship behavior by motion cues and activation of male-specific P1 neurons. Proc. Natl. Acad. Sci. U.S.A. 109, 10065– 10070 (2012). 22645338 PMC3382505
  102. [118]H. Li, F. Horns, B. Wu, Q. Xie, J. Li, T. Li, D. J. Luginbuhl, S. R. Quake, L. Luo, Classifying Drosophila olfactory projection neuron subtypes by single-cell RNA sequencing. Cell 171, 1206– 1220.e22 (2017). 29149607 PMC6095479
  103. [120]L. Luo, Y. J. Liao, L. Y. Jan, Y. N. Jan, Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787– 1802 (1994). 7958857
  104. [121]N. Yapici, Y.-J. Kim, C. Ribeiro, B. J. Dickson, A receptor that mediates the post-mating switch in Drosophila reproductive behaviour. Nature 451, 33– 37 (2008). 18066048
  105. [123]R. A. Baines, L. Seugnet, A. Thompson, P. M. Salvaterra, M. Bate, Regulation of synaptic connectivity: Levels of fasciclin II influence synaptic growth in the Drosophila CNS. J. Neurosci. 22, 6587– 6595 (2002). 12151538 PMC6758157
  106. [124]C. R. von Reyn, P. Breads, M. Y. Peek, G. Z. Zheng, W. R. Williamson, A. L. Yee, A. Leonardo, G. M. Card, A spike-timing mechanism for action selection. Nat. Neurosci. 17, 962– 970 (2014). 24908103
  107. [125]B. D. Pfeiffer, J. W. Truman, G. M. Rubin, Using translational enhancers to increase transgene expression in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 109, 6626– 6631 (2012). 22493255 PMC3340069
  108. [126]R. A. Bohm, W. P. Welch, L. K. Goodnight, L. W. Cox, L. G. Henry, T. C. Gunter, H. Bao, B. Zhang, A genetic mosaic approach for neural circuit mapping in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 107, 16378– 16383 (2010). 20810922 PMC2941334
  109. [127]N. C. Klapoetke, Y. Murata, S. S. Kim, S. R. Pulver, A. Birdsey-Benson, Y. K. Cho, T. K. Morimoto, A. S. Chuong, E. J. Carpenter, Z. Tian, J. Wang, Y. Xie, Z. Yan, Y. Zhang, B. Y. Chow, B. Surek, M. Melkonian, V. Jayaraman, M. Constantine-Paton, G. K.-S. Wong, E. S. Boyden, Independent optical excitation of distinct neural populations. Nat. Methods 11, 338– 346 (2014). 24509633 PMC3943671
  110. [128]P. Stockinger, D. Kvitsiani, S. Rotkopf, L. Tirián, B. J. Dickson, Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795– 807 (2005). 15935765
  111. [129]E. J. Rideout, A. J. Dornan, M. C. Neville, S. Eadie, S. F. Goodwin, Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat. Neurosci. 13, 458– 466 (2010). 20305646 PMC3092424
  112. [130]J. Y. Yu, M. I. Kanai, E. Demir, G. S. X. E. Jefferis, B. J. Dickson, Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr. Biol. 20, 1602– 1614 (2010). 20832315
  113. [131]H. Toda, X. Zhao, B. J. Dickson, The Drosophila female aphrodisiac pheromone activates ppk23(+) sensory neurons to elicit male courtship behavior. Cell Rep. 1, 599– 607 (2012). 22813735
  114. [132]E. Starostina, T. Liu, V. Vijayan, Z. Zheng, K. K. Siwicki, C. W. Pikielny, A Drosophila DEG/EnaC subunit functions specifically in gustatory neurons required for male courtship behavior. J. Neurosci. 32, 4665– 4674 (2012). 22457513 PMC3324785
  115. [133]J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J.-Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, A. Cardona, Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676– 682 (2012). 22743772 PMC3855844
  116. [134]Y. Wan, H. Otsuna, H. A. Holman, B. Bagley, M. Ito, A. K. Lewis, M. Colasanto, G. Kardon, K. Ito, C. Hansen, FluoRender: Joint freehand segmentation and visualization for many-channel fluorescence data analysis. BMC Bioinformatics 18, 280 (2017). 28549411 PMC5446689
  117. [135]M. Kabra, A. A. Robie, M. Rivera-Alba, S. Branson, K. Branson, JAABA: Interactive machine learning for automatic annotation of animal behavior. Nat. Methods 10, 64– 67 (2013). 23202433
  118. [136]A. Dobin, C. A. Davis, F. Schlesinger, J. Drenkow, C. Zaleski, S. Jha, P. Batut, M. Chaisson, T. R. Gingeras, STAR: Ultrafast universal RNA-seq aligner. Bioinformatics 29, 15– 21 (2013). 23104886 PMC3530905
  119. [137]S. Heinz, C. Benner, N. Spann, E. Bertolino, Y. C. Lin, P. Laslo, J. X. Cheng, C. Murre, H. Singh, C. K. Glass, Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576– 589 (2010). 20513432 PMC2898526
  120. [138]M. D. Robinson, D. J. McCarthy, G. K. Smyth, edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139– 140 (2010). 19910308 PMC2796818

Cited by

Sorted by citations

Authors
Ishii, K., Cortese, M., Leng, X., Shokhirev, M. N., & Asahina, K.
Affiliations
Salk Institute for Biological Studies (US)
Corresponding author
Asahina, Kenta
Venue
Science Advances
Published
2022-09-09
Volume
8
Issue
36
Pages
eabg3203-eabg3203
ISSN
2375-2548 (ISSN-L)
OpenAlex
W4294884840
Cited by
16
References
12
Citations by year
2026: 6 · 2025: 6 · 2024: 2 · 2023: 2
FWCI
1.11
Type
journal article
Language
en
Open access
Licence
cc-by-nc
Locations
  • Science Advances (publishedVersion, cc-by-nc)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (P40OD018537)
  • Japan Society for the Promotion of Science (22K06309)
  • National Institute of General Medical Sciences (R35GM119844)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
aggression, social experience, Drosophila, octopaminergic neurons, loss-of-function mutations, cell type-specific transcriptomics, social behavior
MeSH terms
Aggression, Animals, Drosophila, Female, Humans, Male, Neurosciences, Social Behavior, Drosophila Proteins

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