Social Opportunity Causes Rapid Transcriptional Changes in the Social Behaviour Network of the Brain in an African Cichlid Fish

Journal of Neuroendocrinology

Volumn 25, Issue 2, 2013, Pages 145-157

  Maruska, K P ^a,b   Zhang, A ^a   Neboori, A ^a   Fernald, R D ^a  

^a STANFORD UNIVERSITY   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

A statotilapia burtoni; Dominance; Immediate early gene; Social behaviour network; Steroid receptor; Teleost

Indexed keywords

ANDROGEN RECEPTOR; AROMATASE; ESTROGEN RECEPTOR; MESSENGER RNA; STEROID HORMONE; STEROID RECEPTOR;

ADAPTIVE BEHAVIOR; AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTATOTILAPIA BURTONI; BRAIN NUCLEUS; BRAIN REGION; CICHLID; CONTROLLED STUDY; FEMALE; HORMONE RELEASE; IMMEDIATE EARLY GENE; MALE; MICRODISSECTION; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; REPRODUCTION; REWARD; SEPTUM NUCLEUS; SIGNAL TRANSDUCTION; SOCIAL BEHAVIOR; SOCIAL BEHAVIOR NETWORK; SOCIAL DOMINANCE; SOCIAL NETWORK; SOCIAL STATUS;

AGGRESSION; ANIMALS; BEHAVIOR, ANIMAL; BRAIN; CICHLIDS; GONADAL STEROID HORMONES; MALE; MODELS, BIOLOGICAL; NERVE NET; REPRODUCTION; SOCIAL BEHAVIOR; SOCIAL DOMINANCE; TRANSCRIPTION, GENETIC;

EID: 84873022282     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2012.02382.x     Document Type: Article

References (72)

1. Maruska KP, Fernald RD. Social regulation of gene expression in the hypothalamic-pituitary-gonadal axis. Physiology 2011; 26: 412-423.
2. Robinson GE, Fernald RD, Clayton DF. Genes and social behavior. Science 2008; 322: 896-900.
3. Kaufmann JH. On the definitions and functions of dominance and territoriality. Biol Rev 1983; 58: 1-20.
4. Fernald RD. Social regulation of reproduction: what changes and why? Horm Brain Behav 2009; 1: 683-691.
5. O'Connell LA, Hofmann HA. Genes, hormones, and circuits: an integrative approach to study the evolution of social behavior. Front Neuroendocrinol 2011; 32: 320-335.
6. Fernald RD, Hirata NR. Field study of Haplochromis burtoni: quantitative behavioral observations. Animal Behav 1977; 25: 964-975.
7. 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: 3041-3056.
8. Sneddon LU, Schmidt R, Fang Y, Cossins AR. Molecular correlates of social dominance: a novel role for ependymin in aggression. PLoS ONE 2011; 6: e18181.
9. O'Connell LA, Hofmann HA. The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 2011; 519: 3599-3639.
10. Newman SW. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann NY Acad Sci 1999; 877: 242-257.
11. Goodson JL. The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 2005; 48: 11-22.
12. Crews D. The development of phenotypic plasticity: where biology and psychology meet. Dev Psychobiol 2003; 43: 1-10.
13. Goodson JL, Bass AH. Vocal-acoustic circuitry and descending vocal pathways in teleost fish: convergence with terrestrial vertebrates reveals conserved traits. J Comp Neurol 2002; 448: 298-322.
14. Desjardins JK, Klausner JQ, Fernald RD. Female genomic response to mate information. Proc Natl Acad Sci USA 2010; 107: 21176-21180.
15. Hoke KL, Ryan MJ, Wilczynski W. Social cues shift functional connectivity in the hypothalamus. Proc Natl Acad Sci USA 2005; 102: 10712-10717.
16. Pfaus JG, Heeb MM. Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res Bull 1997; 44: 397-407.
17. Riters LV, Teague DP, Schroeder MB, Cummings SE. Vocal production in different social contexts relates to variation in immediate early gene immunoreactivity within and outside of the song control system. Behav Brain Res 2004; 155: 307-318.
18. Burmeister SS, Jarvis ED, Fernald RD. Rapid behavioral and genomic responses to social opportunity. PLoS Biol 2005; 3: e363.
19. Kovacs KJ. Measurement of immediate-early gene activation- c-fos and beyond. J Neuroendocrinol 2008; 20: 665-672.
20. Luckman SM, Dyball RE, Leng G. Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity. J Neurosci 1994; 14: 4825-4830.
21. Clayton DF. The genomic action potential. Neurobiol Learn Mem 2000; 74: 185-216.
22. Hofmann HA. The neuroendocrine action potential. Winner of the 2008 Frank Beach Award in Behavioral Neuroendocrinology. Horm Behav 2010; 58: 555-562.
23. Hofmann HA, Benson ME, Fernald RD. Social status regulates growth rate: consequences for life-history strategies. Proc Natl Acad Sci USA 1999; 96: 14171-14176.
24. Maruska KP, Fernald RD. Behavioral and physiological plasticity: rapid changes during social ascent in an African cichlid fish. Horm Behav 2010; 58: 230-240.
25. Maruska KP, Fernald RD. Plasticity of the reproductive axis caused by social status change in an African cichlid fish: II. testicular gene expression and spermatogenesis. Endocrinology 2011; 152: 291-302.
26. Maruska KP, Levavi-Sivan B, Biran J, Fernald RD. Plasticity of the reproductive axis caused by social status change in an African cichlid fish: I. pituitary gonadotropins. Endocrinology 2011; 152: 281-290.
27. Kustan JM, Maruska KP, Fernald RD. Subordinate male cichlids retain reproductive competence during social suppression. Proc R Soc B 2012; 279: 434-443.
28. White SA, Nguyen T, Fernald RD. Social regulation of gonadotropin-releasing hormone. J Exp Biol 2002; 205: 2567-2581.
29. Fernald RD, Shelton LC. The organization of the diencephalon and the pretectum in the cichlid fish, Haplochromis burtoni. J Comp Neurol 1985; 238: 202-217.
30. Burmeister SS, Munshi RG, Fernald RD. Cytoarchitecture of a cichlid fish telencephalon. Brain Behav Evol 2009; 74: 110-120.
31. Munchrath LA, Hofmann HA. Distribution of sex steroid hormone receptors in the brain of an African cichlid fish, Astatotilapia burtoni. J Comp Neurol 2010; 518: 3302-3326.
32. Munoz-Cueto JA, Sarasquete C, Zohar AH, Kah O. An Atlas of the Brain of the Gilthead Seabream (Sparus aurata) College Park, MD: Maryland Sea Grant, 2001.
33. Wulliman MF, Rupp B, Reichert H. Neuroanatomy of the Zebrafish Brain: A Topological Atlas, Basel: Birkhauser Verlag, 1996.
34. Maler L, Sas E, Johnston S, Ellis W. An atlas of the brain of the electric fish Apteronotus leptorhynchus. J Chem Neuroanat 1991; 4: 1-38.
35. Wullimann MF, Mueller T. Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J Comp Neurol 2004; 475: 143-162.
36. Moore FL, Lowry CA. Comparative neuroanatomy of vasotocin and vasopressin in amphibians and other vertebrates. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 1998; 119: 251-260.
37. Maruska KP, Fernald RD. Steroid receptor expression in the fish inner ear varies with sex, social status, and reproductive state. BMC Neurosci 2010; 11: 58.
38. Zhao S, Fernald RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J Comput Biol 2005; 12: 1047-1064.
39. Burmeister SS, Kailasanath V, Fernald RD. Social dominance regulates androgen and estrogen receptor gene expression. Horm Behav 2007; 51: 164-170.
40. Maruska KP, Fernald RD. Reproductive status regulates expression of sex steroid and GnRH receptors in the olfactory bulb. Behav Brain Res 2010; 213: 208-217.
41. Burmeister SS, Fernald RD. Evolutionary conservation of the egr-1 immediate-early gene response in a teleost. J Comp Neurol 2005; 481: 220-232.
42. Wingfield JC, Hegner R, Dufty A Jr, Ball GF. The 'challenge hypothesis': theoretical implications for patterns of testosterone secretion, mating system, and breeding strategies. Am Nat 1990; 136: 829-846.
43. Huffman LS, Mitchell MM, O'Connell LA, Hofmann HA. Rising StARs: behavioral, hormonal, and molecular responses to social challenge and opportunity. Horm Behav 2012; 61: 631-641.
44. Forlano PM, Bass AH. Neural and hormonal mechanisms of reproductive-related arousal in fishes. Horm Behav 2010; 59: 616-629.
45. Lord LD, Bond J, Thompson RR. Rapid steroid influences on visually guided sexual behavior in male goldfish. Horm Behav 2009; 56: 519-526.
46. O'Connell LA, Hofmann HA. Social status predicts how sex steroid receptors regulate complex behavior across levels of biological organization. Endocrinology 2012; 153: 1341-1351.
47. Bliss SP, Navratil AM, Xie J, Roberson MS. GnRH signaling, the gonadotrope and endocrine control of fertility. Front Neuroendocrinol 2010; 31: 322-340.
48. Mayer SI, Willars GB, Nishida E, Thiel G. Elk-1, CREB, and MKP-1 regulate Egr-1 expression in gonadotropin-releasing hormone stimulated gonadotrophs. J Cell Biochem 2008; 105: 1267-1278.
49. Martinez M, Calvo-Torrent A, Herbert J. Mapping brain response to social stress in rodents with c-fos expression: a review. Stress 2002; 5: 3-13.
50. Kollack-Walker S, Watson SJ, Akil H. Social stress in hamsters: defeat activates specific neurocircuits within the brain. J Neurosci 1997; 17: 8842-8855.
51. Soma KK, Tramontin AD, Wingfield JC. Oestrogen regulates male aggression in the non-breeding season. Proc Biol Sci 2000; 267: 1089-1096.
52. Ogawa S, Chester AE, Hewitt SC, Walker VR, Gustafsson JA, Smithies O, Korach KS, Pfaff DW. Abolition of male sexual behaviors in mice lacking estrogen receptors alpha and beta (alpha beta ERKO). Proc Natl Acad Sci USA 2000; 97: 14737-14741.
53. Cornil CA, Dalla C, Papadopoulou-Daifoti Z, Baillien M, Balthazart J. Estradiol rapidly activates male sexual behavior and affects brain monoamine levels in the quail brain. Behav Brain Res 2006; 166: 110-123.
54. Remage-Healey L, Bass AH. A rapid neuromodulatory role for steroid hormones in the control of reproductive behavior. Brain Res 2006; 1126: 27-35.
55. Taziaux M, Keller M, Bakker J, Balthazart J. Sexual behavior activity tracks rapid changes in brain estrogen concentrations. J Neurosci 2007; 27: 6563-6572.
56. Imwalle DB, Scordalakes EM, Rissman EF. Estrogen receptor alpha influences socially motivated behaviors. Horm Behav 2002; 42: 484-491.
57. Ogawa S, Lubahn DB, Korach KS, Pfaff DW. Behavioral effects of estrogen receptor gene disruption in male mice. Proc Natl Acad Sci USA 1997; 94: 1476-1481.
58. Trainor BC, Greiwe KM, Nelson RJ. Individual differences in estrogen receptor alpha in select brain nuclei are associated with individual differences in aggression. Horm Behav 2006; 50: 338-345.
59. Cornil CA, Ball GF, Balthazart J. Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from? Brain Res 2006; 1126: 2-26.
60. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan LP, Alves SE. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 2001; 429: 355-371.
61. Srivastava DP, Waters EM, Mermelstein PG, Kramar EA, Shors TJ, Liu F. Rapid estrogen signaling in the brain: implications for the fine-tuning of neuronal circuitry. J Neurosci 2011; 31: 16056-16063.
62. Forlano PM, Schlinger BA, Bass AH. Brain aromatase: new lessons from non-mammalian model systems. Front Neuroendocrinol 2006; 27: 247-274.
63. Forlano PM, Bass AH. Seasonal plasticity of brain aromatase mRNA expression in glia: divergence across sex and vocal phenotypes. J Neurobiol 2005; 65: 37-49.
64. Handa RJ, Ogawa S, Wang JM, Herbison AE. Roles for estrogen receptor beta in adult brain function. J Neuroendocrinol 2012; 24: 160-173.
65. Lin D, Boyle MP, Dollar P, Lee H, Lein ES, Perona P, Anderson DJ. Functional identification of an aggression locus in the mouse hypothalamus. Nature 2011; 470: 221-226.
66. Fuxjager MJ, Forbes-Lorman RM, Coss DJ, Auger CJ, Auger AP, Marler CA. Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proc Natl Acad Sci USA 2010; 107: 12393-12398.
67. Hirschenhauser K, Wittek M, Johnston P, Mostl E. Social context rather than behavioral output or winning modulates post-conflict testosterone responses in Japanese quail (Coturnix japonica). Physiol Behav 2008; 95: 457-463.
68. Juntti SA, Tollkuhn J, Wu MV, Fraser EJ, Soderborg T, Tan S, Honda S, Harada N, Shah NM. The androgen receptor governs the execution, but not programming, of male sexual and territorial behaviors. Neuron 2010; 66: 260-272.
69. Remage-Healey L, Maidment NT, Schlinger BA. Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 2008; 11: 1327-1334.
70. Tremere LA, Pinaud R. Brain-generated estradiol drives long-term optimization of auditory coding to enhance the discrimination of communication signals. J Neurosci 2011; 31: 3271-3289.
71. Pradhan DS, Newman AE, Wacker DW, Wingfield JC, Schlinger BA, Soma KK. Aggressive interactions rapidly increase androgen synthesis in the brain during the non-breeding season. Horm Behav 2010; 57: 381-389.
72. Maney DL, Pinaud R. Estradiol-dependent modulation of auditory processing and selectivity in songbirds. Front Neuroendocrinol 2011; 32: 287-302.