Behavioral and brain- transcriptomic synchronization between the two opponents of a fighting pair of the fish Betta splendens


Autoři: Trieu-Duc Vu aff001;  Yuki Iwasaki aff002;  Shuji Shigenobu aff007;  Akiko Maruko aff001;  Kenshiro Oshima aff001;  Erica Iioka aff002;  Chao-Li Huang aff008;  Takashi Abe aff009;  Satoshi Tamaki aff010;  Yi-Wen Lin aff005;  Chih-Kuan Chen aff004;  Mei-Yeh Lu aff004;  Masaru Hojo aff005;  Hao-Ven Wang aff005;  Shun-Fen Tzeng aff005;  Hao-Jen Huang aff005;  Akio Kanai aff010;  Takashi Gojobori aff011;  Tzen-Yuh Chiang aff005;  H. Sunny Sun aff012;  Wen-Hsiung Li aff004;  Norihiro Okada aff001
Působiště autorů: School of Pharmacy, Kitasato University, Tokyo, Japan aff001;  Foundation for Advancement of International Science, Tsukuba, Japan aff002;  Life Sciences and Biotechnology Dept, Tokyo Institute of Technology, Tokyo, Japan aff003;  Biodiversity Research Center, Academia Sinica, Taipei, Taiwan aff004;  Department of Life Sciences, National Cheng Kung University, Tainan, Taiwan aff005;  Nagahama Institute of Bio-Science and Technology, Nagahama, Japan aff006;  National Institute for Basic Biology, Okazaki, Japan aff007;  Institute of Tropical Plant Sciences, National Cheng Kung University, Tainan, Taiwan aff008;  Graduate School of Science and Technology, Niigata University, Niigata, Japan aff009;  Institute for Advanced Biosciences, Keio University, Yamagata, Japan aff010;  Computational Bioscience Research Center, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia aff011;  Institute of Molecular Medicine, National Cheng Kung University, Tainan, Taiwan aff012;  Department of Ecology and Evolution, University of Chicago, IL, United States of America aff013
Vyšlo v časopise: Behavioral and brain- transcriptomic synchronization between the two opponents of a fighting pair of the fish Betta splendens. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008831
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008831

Souhrn

Conspecific male animals fight for resources such as food and mating opportunities but typically stop fighting after assessing their relative fighting abilities to avoid serious injuries. Physiologically, how the fighting behavior is controlled remains unknown. Using the fighting fish Betta splendens, we studied behavioral and brain-transcriptomic changes during the fight between the two opponents. At the behavioral level, surface-breathing, and biting/striking occurred only during intervals between mouth-locking. Eventually, the behaviors of the two opponents became synchronized, with each pair showing a unique behavioral pattern. At the physiological level, we examined the expression patterns of 23,306 brain transcripts using RNA-sequencing data from brains of fighting pairs after a 20-min (D20) and a 60-min (D60) fight. The two opponents in each D60 fighting pair showed a strong gene expression correlation, whereas those in D20 fighting pairs showed a weak correlation. Moreover, each fighting pair in the D60 group showed pair-specific gene expression patterns in a grade of membership analysis (GoM) and were grouped as a pair in the heatmap clustering. The observed pair-specific individualization in brain-transcriptomic synchronization (PIBS) suggested that this synchronization provides a physiological basis for the behavioral synchronization. An analysis using the synchronized genes in fighting pairs of the D60 group found genes enriched for ion transport, synaptic function, and learning and memory. Brain-transcriptomic synchronization could be a general phenomenon and may provide a new cornerstone with which to investigate coordinating and sustaining social interactions between two interacting partners of vertebrates.

Klíčová slova:

Animal behavior – Fish physiology – Gene expression – Learning and memory – MAPK signaling cascades – RNA sequencing – Transcriptome analysis – Zebrafish


Zdroje

1. Darwin C. On the Origin of Species by Means of Natural Selection. Murray, London. 1859.

2. Arnott G, Elwood R. Information gathering and decision making about resource value in animal contests. Animal Behavior. 2008;76(3):529–42.

3. Arnott G, Elwood R. Assessment of fighting ability in animal contests. Anim Behaviour. 2009;77(5):991–1004.

4. Lindenfors P, Tullberg BS. Evolutionary aspects of aggression the importance of sexual selection. Adv Genet. 2011; 75:7–22. doi: 10.1016/B978-0-12-380858-5.00009-5 22078475

5. Taborsky B, Oliveira RF. Social competence: an evolutionary approach. Trends Ecol Evol. 2012;27(12):679–88. doi: 10.1016/j.tree.2012.09.003 23040461

6. Oliveira RF, Simoes JM, Teles MC, Oliveira CR, Becker JD, Lopes JS. Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain. Proc Natl Acad Sci U S A. 2016;113(5): E654–61. doi: 10.1073/pnas.1514292113 26787876

7. Oliveira RF, McGregor PK, Latruffe C, PRSL B, Oliveira RF, McGregor PK, et al. Know thine enemy: fighting fish gather information from observing conspecific interactions. 1998:1045–9.

8. Lorenz K. On aggression. Routledge London & New York. 2005.

9. Kravitz EA, Huber R. Aggression in invertebrates. Curr Opin Neurobiol. 2003;13(6):736–43. doi: 10.1016/j.conb.2003.10.003 14662376

10. Tate M, McGoran RE, White CR. Life in a bubble: the role of the labyrinth organ in determining territory, mating and aggressive behaviours in anabantoids. 2017; 44:723–49.

11. Lin C-p, Lin H-c, Zoology B. Morphological and Biochemical Variations in the Gills of 12 Aquatic Air-Breathing Anabantoid Fish. 2014(May).

12. Monvises A, Nuangsaeng B, Sriwattanarothai N, Panijpan B. The Siamese fighting fish: well-known generally but little-known scientifically. SienceAsia. 2009; 35:8–16.

13. Simpson MJA. The Display of the Siamese Fighting Fish, Betta splendens. Animal Behavior Monographs. 1968;1(1): i-viii, 1–73.

14. Doutrelant C, McGregor PK, Oliveira RF. The effect of an audience on intrasexual communication in male Siamese fighting fish, Betta splendens. Behavioral Ecology. 2001;12(3):283–6.

15. Processes B. Type of intruder and reproductive phase influence male territorial defense in wild- caught Siamese fighting fish, Betta splendens. 2003.

16. Castro N, Ros A, Becker K, Oliveira R. Metabolic costs of aggressive behavior in the Siamese fighting fish, Betta splendens2006. 474–80 p.

17. Alton LA, Portugal SJ, White CR. Balancing the competing requirements of air-breathing and display behaviour during male-male interactions in Siamese fighting fish Betta splendens. Comp Biochem Physiol A Mol Integr Physiol. 2013;164(2):363–7. doi: 10.1016/j.cbpa.2012.11.012 23178457

18. Justus KT, Mendelson TC. Male preference for conspeci fi c mates is stronger than females’ in Betta. Behavioural Processes. 2018;151(February):6–10.

19. Schneider H. Measuring Agonistic Behavior in Zebrafish. Zebrafish Neurobehavioral Protocols. 2011; 51:125–34.

20. Matos RJ, McGregor PK. The effect of the sex of an audience on male-male displays of Siamese fighting fish (Betta splendens). Behaviour. 2002;138(9):1211–21.

21. Dzieweczynski TL, Leopard AK. The effects of stimulus type on consistency of responses to conflicting stimuli in Siamese fighting fish. Behav Processes. 2010;85(2):83–9. doi: 10.1016/j.beproc.2010.06.011 20600699

22. Verbeek P, Iwamoto T, Murakami N. Differences in aggression between wild-type and domesticated fighting fish are context dependent. Anim Behaviour. 2007;73(1):75–83.

23. Larson ET, O'Malley DM, Melloni RH Jr. Aggression and vasotocin are associated with dominant-subordinate relationships in zebrafish. Behav Brain Res. 2006;167(1):94–102. doi: 10.1016/j.bbr.2005.08.020 16213035

24. Clotfelter ED, O'Hare EP, McNitt MM, Carpenter RE, Summers CH. Serotonin decreases aggression via 5-HT1A receptors in the fighting fish Betta splendens. Pharmacol Biochem Behav. 2007;87(2):222–31. doi: 10.1016/j.pbb.2007.04.018 17553555

25. Clotfelter ED, McNitt MM, Carpenter RE, Summers CH. Modulation of monoamine neurotransmitters in fighting fish Betta splendens exposed to waterborne phytoestrogens. 2010:933–43.

26. Yang W, Wang Y, Zhu C, et al. De novo transcriptomic characterization of Betta splendens for identifying sex-biased genes potentially involved in aggressive behavior modulation and EST-SSR maker development. bioRxiv; 2018. doi: 10.1101/355354

27. Renn SC, Aubin-Horth N, Hofmann HA. Fish and chips: functional genomics of social plasticity in an African cichlid fish. J Exp Biol. 2008;211(Pt 18):3041–56. doi: 10.1242/jeb.018242 18775941

28. Filby AL, Paull GC, Hickmore TF, Tyler CR. Unravelling the neurophysiological basis of aggression in a fish model. BMC Genomics. 2010;11:498. doi: 10.1186/1471-2164-11-498 20846403

29. Sneddon LU, Margareto J, Cossins AR. The use of transcriptomics to address questions in behaviour: production of a suppression subtractive hybridisation library from dominance hierarchies of rainbow trout. Physiol Biochem Zool. 2005;78(5):695–705. doi: 10.1086/432141 16052453

30. Greenwood AK, Wark AR, Fernald RD, Hofmann HA. Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish. Proc Biol Sci. 2008;275(1649):2393–402. doi: 10.1098/rspb.2008.0622 18628117

31. Kroes RA, Panksepp J, Burgdorf J, Otto NJ, Moskal JR. Modeling depression: social dominance-submission gene expression patterns in rat neocortex. Neuroscience. 2006;137(1):37–49. doi: 10.1016/j.neuroscience.2005.08.076 16289586

32. Fan G, Chan J, Ma K, Yang B, Zhang H, Yang X, et al. Chromosome-level reference genome of the Siamese fighting fish Betta splendens, a model species for the study of aggression. Gigascience. 2018;7(11).

33. Axelrod R, Hamilton WD. The evolution of cooperation. science. 1981;211(4489):1390–6. doi: 10.1126/science.7466396 7466396

34. Bshary R, Grutter AS. Asymmetric cheating opportunities and partner control in a cleaner fish mutualism. Animal Behaviour. 2002;63(3):547–55.

35. Soares MC, Paula JR, Bshary R. Serotonin blockade delays learning performance in a cooperative fish. Animal cognition. 2016;19(5):1027–30. doi: 10.1007/s10071-016-0988-z 27107861

36. Paula JR, Messias JP, Grutter AS, Bshary R, Soares MC. The role of serotonin in the modulation of cooperative behavior. Behavioral Ecology. 2015;26(4):1005–12.

37. Cardoso SC, Paitio JR, Oliveira RF, Bshary R, Soares MC. Arginine vasotocin reduces levels of cooperative behaviour in a cleaner fish. Physiology & behavior. 2015;139:314–20.

38. Kingsbury L, Huang S, Wang J, Gu K, Golshani P, Wu YE. Correlated Neural Activity and Encoding of Behavior across Brains of Socially Interacting Animals Correlated Neural Activity and Encoding of Behavior across Brains of Socially Interacting Animals. Cell. 2019:1–18.

39. Zhang W, Yartsev MM. Article Correlated Neural Activity across the Brains of Socially Interacting Bats. Cell. 2019:1–16.

40. Kandel ER, Schwartz JH, Jessell TM. Principles of Neural Science, Fifth Edition. McGraw-Hill Companies, New York. 2000;4:1227–46.

41. Clayton DF. The genomic action potential. Neurobiol Learn Mem. 2000;74(3):185–216. doi: 10.1006/nlme.2000.3967 11031127

42. Cummings ME, Larkins-Ford J, Reilly CR, Wong RY, Ramsey M, Hofmann HA. Sexual and social stimuli elicit rapid and contrasting genomic responses. Proc Biol Sci. 2008;275(1633):393–402. doi: 10.1098/rspb.2007.1454 18055387

43. Maruska KP, Zhang A, Neboori A, Fernald RD. Social opportunity causes rapid transcriptional changes in the social behaviour network of the brain in an African cichlid fish. J Neuroendocrinol. 2013;25(2):145–57. doi: 10.1111/j.1365-2826.2012.02382.x 22958303

44. Oliveira RF, Silva JF, Simoes JM. Fighting zebrafish: characterization of aggressive behavior and winner-loser effects. Zebrafish. 2011;8(2):73–81. doi: 10.1089/zeb.2011.0690 21612540

45. Alaux C, Sinha S, Hasadsri L, Hunt GJ, Guzman-Novoa E, DeGrandi-Hoffman G, et al. Honey bee aggression supports a link between gene regulation and behavioral evolution. Proc Natl Acad Sci U S A. 2009;106(36):15400–5. doi: 10.1073/pnas.0907043106 19706434

46. Chandrasekaran S, Ament SA, Eddy JA, Rodriguez-Zas SL, Schatz BR, Price ND, et al. Behavior-specific changes in transcriptional modules lead to distinct and predictable neurogenomic states. Proc Natl Acad Sci U S A. 2011;108(44):18020–5. doi: 10.1073/pnas.1114093108 21960440

47. Burmeister SS, Jarvis ED, Fernald RD. Rapid behavioral and genomic responses to social opportunity. PLoS Biol. 2005;3(11): e363. doi: 10.1371/journal.pbio.0030363 16216088

48. Okuno H. Regulation and function of immediate-early genes in the brain: beyond neuronal activity markers. Neuroscience research. 2011;69(3):175–86. doi: 10.1016/j.neures.2010.12.007 21163309

49. Ghosh A, Greenberg ME. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science. 1995;268(5208):239–47. doi: 10.1126/science.7716515 7716515

50. Iii RJK, Govindarajan A, Jung H-y, Kang H, Tonegawa S. Translational Control by MAPK Signaling in Long-Term Synaptic Plasticity and Memory. 2004; 116:467–79.

51. Robinson GE, Ben-Shahar Y. Social behavior and comparative genomics: new genes or new gene regulation? Genes Brain Behav. 2002;1(4):197–203. doi: 10.1034/j.1601-183x.2002.10401.x 12882364

52. Howard MW, Rizzuto DS, Caplan JB, Madsen JR, Lisman J, Aschenbrenner-Scheibe R, et al. Gamma oscillations correlate with working memory load in humans. Cereb Cortex. 2003;13(12):1369–74. doi: 10.1093/cercor/bhg084 14615302

53. Chou MY, Amo R, Kinoshita M, Cherng BW, Shimazaki H, Agetsuma M, et al. Social conflict resolution regulated by two dorsal habenular subregions in zebrafish. Science. 2016;352(6281):87–90. doi: 10.1126/science.aac9508 27034372

54. Enquist M, Leimar O, Ljungberg T, Mallner Y, Segerdahl N. A test of the sequential assessment game: fighting in the cichlid fish Nannacara anomala. Animal Behavior. 1990;40(1):1–14.

55. Gotceitas V, Godin JGJ. Foraging under the Risk of Predation in Juvenile Atlantic Salmon (Salmo salar L.): Effects of Social Status and Hunger. Behavioral Ecology and Sociobiology. 1991;29(4):255–61.

56. Pellegrino G, Fadiga L, Fogassi L. Understanding motor events: a physiological. Experimental brain …. 1992:176–80.

57. Nakayama S, Johnstone RA, Manica A. Temperament and hunger interact to determine the emergence of leaders in pairs of foraging fish. PLoS One. 2012;7(8):e43747. doi: 10.1371/journal.pone.0043747 22952753

58. Nakayama S, Stumpe MC, Manica A, Johnstone RA. Experience overrides personality differences in the tendency to follow but not in the tendency to lead. Proc Biol Sci. 2013;280(1769):20131724. doi: 10.1098/rspb.2013.1724 23986110

59. Reale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. Integrating animal temperament within ecology and evolution. Biological reviews of the Cambridge Philosophical Society. 2007;82(2):291–318. doi: 10.1111/j.1469-185X.2007.00010.x 17437562

60. Croft DP, James R, Ward AJ, Botham MS, Mawdsley D, Krause J. Assortative interactions and social networks in fish. Oecologia. 2005;143(2):211–9. doi: 10.1007/s00442-004-1796-8 15682346

61. Firth JA, Cole EF, Ioannou CC, Quinn JL, Aplin LM, Culina A, et al. Personality shapes pair bonding in a wild bird social system. Nat Ecol Evol. 2018;2(11):1696–9. doi: 10.1038/s41559-018-0670-8 30275466

62. Bekinschtein P, Cammarota M, Igaz LM, Bevilaqua LR, Izquierdo I, Medina JH. Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus. Neuron. 2007;53(2):261–77. doi: 10.1016/j.neuron.2006.11.025 17224407

63. Safe S, Jin UH, Morpurgo B, Abudayyeh A, Singh M, Tjalkens RB. Nuclear receptor 4A (NR4A) family—orphans no more. J Steroid Biochem Mol Biol. 2016;157:48–60. doi: 10.1016/j.jsbmb.2015.04.016 25917081

64. Malenka RC, Nicoll RA. Long-term potentiation—a decade of progress? Science. 1999;285(5435):1870–4. doi: 10.1126/science.285.5435.1870 10489359

65. Cui WW, Low SE, Hirata H, Saint-Amant L, Geisler R, Hume RI, et al. The zebrafish shocked gene encodes a glycine transporter and is essential for the function of early neural circuits in the CNS. J Neurosci. 2005;25(28):6610–20. doi: 10.1523/JNEUROSCI.5009-04.2005 16014722

66. Mills BN, Albert GP, Halterman MW. Expression profiling of the MAP kinase phosphatase family reveals a role for DUSP1 in the glioblastoma stem cell niche. Cancer Microenvironment. 2017;10(1–3):57–68. doi: 10.1007/s12307-017-0197-6 28822081

67. Dolmetsch RE, Pajvani U, Fife K, Spotts JM, & Greenberg ME (2001) Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294(5541):333–339. doi: 10.1126/science.1063395 11598293

68. Wu J, Huang KP, Huang FL. Participation of NMDA-mediated phosphorylation and oxidation of neurogranin in the regulation of Ca2+- and Ca2+/calmodulin-dependent neuronal signaling in the hippocampus. J Neurochem. 2003;86(6):1524–33. doi: 10.1046/j.1471-4159.2003.01963.x 12950461

69. Chi B, Wang Q, Wu G, Tan M, Wang L, Shi M, et al. Aly and THO are required for assembly of the human TREX complex and association of TREX components with the spliced mRNA. Nucleic acids research. 2013;41(2):1294–306. doi: 10.1093/nar/gks1188 23222130

70. Bukhari SA, Saul MC, Seward CH, Zhang H, Bensky M, James N, et al. Temporal dynamics of neurogenomic plasticity in response to social interactions in male threespined sticklebacks. PLoS genetics. 2017;13(7).

71. Saul MC, Seward CH, Troy JM, Zhang H, Sloofman LG, Lu X, et al. Transcriptional regulatory dynamics drive coordinated metabolic and neural response to social challenge in mice. Genome research. 2017;27(6):959–72. doi: 10.1101/gr.214221.116 28356321

72. Saul M.C., Blatti C., Yang W., Bukhari S.A., Shpigler H.Y., Troy J.M., Seward C.H., Sloofman L., Chandrasekaran S., Bell A.M. and Stubbs L., 2019. Cross‐species systems analysis of evolutionary toolkits of neurogenomic response to social challenge. Genes, Brain and Behavior, 18(1), p.e12502.

73. Wong RY, Hofmann HA. Behavioural genomics: an organismic perspective. e LS. 2001 May 30.

74. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC bioinformatics. 2008;9:559. doi: 10.1186/1471-2105-9-559 19114008

75. Dey KK, Hsiao CJ, Stephens M. Visualizing the structure of RNA-seq expression data using grade of membership models. PLoS Genet. 2017;13(3):e1006599. doi: 10.1371/journal.pgen.1006599 28333934

76. Whitfield CW, Cziko A-M, Robinson GE. Gene expression profiles in the brain predict behavior in individual honey bees. Science. 2003;302(5643):296–9. doi: 10.1126/science.1086807 14551438

77. Robinson GE, Fernald RD, Clayton DF. Genes and social behavior. science. 2008;322(5903):896–900. doi: 10.1126/science.1159277 18988841

78. Hofmann HA. Functional genomics of neural and behavioral plasticity. Journal of neurobiology. 2003 Jan;54(1):272–82. doi: 10.1002/neu.10172 12486709

79. Kempadoo KA, Mosharov EV, Choi SJ, Sulzer D, Kandel ER. Dopamine release from the locus coeruleus to the dorsal hippocampus promotes spatial learning and memory. Proc Natl Acad Sci U S A. 2016;113(51):14835–40. doi: 10.1073/pnas.1616515114 27930324

80. Lee JL, Hynds RE. Divergent cellular pathways of hippocampal memory consolidation and reconsolidation. Hippocampus. 2013;23(3):233–44. doi: 10.1002/hipo.22083 23197404

81. Teles MC, Cardoso SD, Oliveira RF. Social plasticity relies on different neuroplasticity mechanisms across the brain social decision-making network in zebrafish. Frontiers in behavioral neuroscience. 2016;10:16. doi: 10.3389/fnbeh.2016.00016 26909029

82. Wong RY, Cummings ME. Expression patterns of neuroligin-3 and tyrosine hydroxylase across the brain in mate choice contexts in female swordtails. Brain, behavior and evolution. 2014;83(3):231–43. doi: 10.1159/000360071 24854097

83. Salamone JD, Yohn SE, Lopez-Cruz L, San Miguel N, Correa M. Activational and effort-related aspects of motivation: neural mechanisms and implications for psychopathology. Brain. 2016;139(Pt 5):1325–47. doi: 10.1093/brain/aww050 27189581

84. O’Connell L.A. and Hofmann H.A., 2012. Evolution of a vertebrate social decision-making network. Science, 336(6085), pp.1154–1157. doi: 10.1126/science.1218889 22654056

85. Desjardins JK, Fernald RD. What do fish make of mirror images? Biology Letters. 2010;6(6):744–7. doi: 10.1098/rsbl.2010.0247 20462889

86. Yoshida K, Saito N, Iriki A, Isoda M. Representation of others' action by neurons in monkey medial frontal cortex. Curr Biol. 2011;21(3):249–53. doi: 10.1016/j.cub.2011.01.004 21256015

87. Breveglieri R, Vaccari FE, Bosco A, Gamberini M, Fattori P, Galletti C. Neurons Modulated by Action Execution and Observation in the Macaque Medial Parietal Cortex. Curr Biol. 2019;29(7):1218–25 e3. doi: 10.1016/j.cub.2019.02.027 30880012

88. Cattaneo L, Fabbri-Destro M, Boria S, Pieraccini C, Monti A, Cossu G, et al. Impairment of actions chains in autism and its possible role in intention understanding. Proc Natl Acad Sci U S A. 2007;104(45):17825–30. doi: 10.1073/pnas.0706273104 17965234

89. Decety J., Bartal I.B.A., Uzefovsky F. and Knafo-Noam A., 2016. Empathy as a driver of prosocial behaviour: highly conserved neurobehavioural mechanisms across species. Philosophical Transactions of the Royal Society B: Biological Sciences, 371(1686), p.20150077.

90. Bailey MR, Simpson EH, Balsam PD. Neural substrates underlying effort, time, and risk-based decision making in motivated behavior. Neurobiol Learn Mem. 2016;133:233–56. doi: 10.1016/j.nlm.2016.07.015 27427327

91. Parkinson C, Kleinbaum AM, Wheatley T. Similar neural responses predict friendship. Nature Communications. 2018.

92. Piazza EA, Hasenfratz L, Hasson U, Lew-Williams C. Infant and adult brains are coupled to the dynamics of natural communication. Psychological Science. 2020;31(1):6–17.

93. Adriaense JEC, Martin JS, Schiestl M, Lamm C, Bugnyar T. Negative emotional contagion and cognitive bias in common ravens (Corvus corax). 2019:1–6.

94. Tyssowski K.M., DeStefino N.R., Cho J.H., Dunn C.J., Poston R.G., Carty C.E., Jones R.D., Chang S.M., Romeo P., Wurzelmann M.K. and Ward J.M., 2018. Different neuronal activity patterns induce different gene expression programs. Neuron, 98(3), pp.530–546. doi: 10.1016/j.neuron.2018.04.001 29681534

95. Goto Y, Grace AA. Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat Neurosci. 2005;8(6):805–12. doi: 10.1038/nn1471 15908948

96. Huber R, Smith K, Delago A, Isaksson K, Kravitz EA. Serotonin and aggressive motivation in crustaceans: altering the decision to retreat. Proc Natl Acad Sci U S A. 1997;94(11):5939–42. doi: 10.1073/pnas.94.11.5939 9159179

97. Saul MC, Majdak P, Perez S, Reilly M, Garland T Jr., Rhodes JS. High motivation for exercise is associated with altered chromatin regulators of monoamine receptor gene expression in the striatum of selectively bred mice. Genes Brain Behav. 2017;16(3):328–41. doi: 10.1111/gbb.12347 27749013

98. Bailey MR, Goldman O, Bello EP, Chohan MO, Jeong N, Winiger V, et al. An Interaction between Serotonin Receptor Signaling and Dopamine Enhances Goal-Directed Vigor and Persistence in Mice. J Neurosci. 2018;38(9):2149–62. doi: 10.1523/JNEUROSCI.2088-17.2018 29367407

99. Dowd M, Joy R. Estimating behavioral parameters in animal movement models using a state‐augmented particle filter. Ecology. 2011;92(3):568–75. doi: 10.1890/10-0611.1 21608465

100. Sengupta S, Bolin JM, Ruotti V, Nguyen BK, Thomson JA, Elwell AL, et al. Single read and paired end mRNA-Seq Illumina libraries from 10 nanograms total RNA. JoVE (Journal of Visualized Experiments). 2011(56):e3340.

101. Embnet M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal. 1994;17(1):10–2.

102. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105–11. doi: 10.1093/bioinformatics/btp120 19289445

103. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–9. doi: 10.1038/nmeth.1923 22388286

104. Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–30. doi: 10.1093/bioinformatics/btt656 24227677

105. Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11(3):R25. doi: 10.1186/gb-2010-11-3-r25 20196867

106. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26(1):139–40. doi: 10.1093/bioinformatics/btp616 19910308

107. Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols. 2009;4(1):44. doi: 10.1038/nprot.2008.211 19131956

108. Supek F, Bošnjak M, Škunca N, Šmuc T. REVIGO summarizes and visualizes long lists of gene ontology terms. PloS one. 2011;6(7).


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