High throughput analysis reveals dissociable gene expression profiles in two independent neural systems involved in the regulation of social behavior

BMC Neuroscience

Volumn 13, Issue 1, 2012, Pages

  Stevenson, Tyler J ^a,d   Replogle, Kirstin ^b,c   Drnevich, Jenny ^c   Clayton, David F ^b,c   Ball, Gregory F ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

Area X; HVC; Microarray; Plasticity; POA; Reproduction; Songbird; Starling

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; STEROID RECEPTOR; THYROID HORMONE RECEPTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN CORTEX; CONTROLLED STUDY; CYTOSKELETON; DNA MICROARRAY; EPIGENETICS; GENE EXPRESSION PROFILING; GENE LOCATION; GENETIC VARIABILITY; HIGH THROUGHPUT SEQUENCING; HYPOTHALAMUS; MALE; MICROTUBULE; NEUROFILAMENT; NONHUMAN; PREOPTIC AREA; REPRODUCTION; SINGING; SOCIAL BEHAVIOR; SONGBIRD;

ANALYSIS OF VARIANCE; ANIMALS; GENE EXPRESSION; HIGH VOCAL CENTER; INTERMEDIATE FILAMENT PROTEINS; LAPAROTOMY; MALE; MICROTUBULES; MITOGEN-ACTIVATED PROTEIN KINASES; NEURAL PATHWAYS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOTOPERIOD; PREOPTIC AREA; RECEPTORS, STEROID; REPRODUCTION; SOCIAL BEHAVIOR; STARLINGS; TRANSCRIPTOME; UP-REGULATION; VOCALIZATION, ANIMAL;

EID: 84867600783     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/1471-2202-13-126     Document Type: Article

References (49)

1. Robinson GE, Fernald RD, Clayton DF. Genes and Social Behavior. Science 2008, 322:896-900. 10.1126/science.1159277, 3052688, 18988841.
2. Robinson GE, Ben-Shahar Y. Social behavior and comparative genomics: new genes or new gene regulation?. Genes Brain Behav. 2002, 1:197-203. 10.1034/j.1601-183X.2002.10401.x, 12882364.
3. Whitfield CW, Cziko AM, Robinson GE. Gene expression profiles in the brain predict behavior in individual honey bees. Science 2003, 302:296-299. 10.1126/science.1086807, 14551438.
4. Renn SCP, 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. 10.1242/jeb.018242, 18775941.
5. Catchpole CK, Slater PJB. Bird Song: Biological Themes and Variations 1995, Cambridge: Cambridge University Press.
6. Nottebohm F, Stokes TM, Leonard CM. Central control of song in the canary. J Comp Neurol 1976, 165:457-486. 10.1002/cne.901650405, 1262540.
7. Aronov D, Andalman AS, Fee MS. A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science 2008, 320:630-634. 10.1126/science.1155140, 18451295.
8. Hessler NA, Doupe AJ. Social context modulates singing-related neural activity in the songbird forebrain. Nature Neurosci 1999, 2:209-211. 10.1038/6306, 10195211.
9. Jarvis ED, Scharff C, Grossman MR, Ramos JA, Nottebohm F. For whom the bird sings. Neuron 1998, 4:775-788.
10. Yu AC, Margoliash D. Temporal hierarchical control of singing in birds. Science 1996, 273:1781-1875.
11. Scharff C, Nottebohm F. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J Neurosci 1991, 11:2896-2913.
12. Bottjer SW, Miesner EA, Arnold AP. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 1984, 224:901-903. 10.1126/science.6719123, 6719123.
13. Nottebohm F. A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 1981, 214:1368. 10.1126/science.7313697, 7313697.
14. Ball GF, Auger CJ, Bernard DJ, Charlier TD, Sartor JJ, Riters LV, Balthazart J. Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann NY Acad Sci 2006, 1016:586-610.
15. Riters LV, Eens M, Pinxten R, Ball GF. Seasonal changes in the densities of α2 noradrenergic receptors are inversely related to changes in testosterone and the volumes of song control nuclei in male European starlings. J Comp Neurol 2002, 444:63-74. 10.1002/cne.10131, 11835182.
16. Stevenson TJ, Lynch KS, Lamba P, Ball GF, Bernard DJ. Cloning of gonadotropin releasing hormone 1 complementary dans in songbirds facilitates dissection of mechanisms mediating seasonal changes in reproduction. Endocrinology 2009, 150:1826-1833. 10.1210/en.2008-1435, 2659271, 19131568.
17. Ball GF, Riters LV, Balthazart J. Neuroendocrinology of song behavior and avian brain plasticity: multiple sites of action of sex steroid hormones. Front Neuroendocrinol 2002, 23:137-178. 10.1006/frne.2002.0230, 11950243.
18. Tramontin AD, Brenowitz EA. Seasonal plasticity in the adult brain. Trends Neurosci 2000, 23:251-258. 10.1016/S0166-2236(00)01558-7, 10838594.
19. Louissaint A, Rao S, Leventhal C, Goldman SA. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 2002, 34:945-960. 10.1016/S0896-6273(02)00722-5, 12086642.
20. Absil P, Pinxten R, Balthazart J, Eens M. Effect of age and testostérone on autumnal neurogenesis in male European starlings (Sturnus vulgaris). Behav Brain Res. 2003 Jul 14, 143(1):15-30. Behav Brain Res, 2003, 143:15-30..
21. Marler R, Peters S, Ball GF, Dufty AM, Wingfield JC. The role of sex steroids in the acquisition and production of birdsong. Nature 1988, 336:770-772. 10.1038/336770a0, 3205304.
22. Nottebohm F. Testosterone triggers growth of brain vocal control nuclei in adult female canaries. Brain Res 1980, 189:429-436. 10.1016/0006-8993(80)90102-X, 7370785.
23. Replogle K, Arnold AP, Ball GF, Band M, Bensch S, Brenowitz EA, Dong S, Drnevich J, Ferris M, George J, Gong G, Hasselquist D, Hernandez AG, Kim R, Lewin HA, Liu L, Lovell PV, Mello CV, Naurin S, Rogriguez-Zas S, Thimmapuram J, Wade J, Clayton DF. The songbird neurogenomics initiative: community based tools and strategies for study of brain gene function and evolution. BMC Genomics 2008, 9:131. 10.1186/1471-2164-9-131, 2329646, 18366674.
24. Dawson A, King VM, Bentley GE, Ball GF. Photoperiodic control of seasonality in birds. J Biol Rhythms 2001, 16:365-382. 10.1177/074873001129002079, 11506381.
25. Lovell PV, Clayton DR, Replogle KL, Mello CV. Birdsong transcriptomics: neurochemical specializations of the oscine song system. PLoS One 2008, 3:e3440. 10.1371/journal.pone.0003440, 2563692, 18941504.
26. Li X, Wang XJ, Tannenhauser J, Podell S, Mukherjeeet P, Hertel M, Biane J, Masuda S, Nottebohm F, Gaasterland T. Genomic resources for songbird research and their use in characterizing gene expression during brain development. Proc Natl Acad Sci 2007, 104:6834-6839. 10.1073/pnas.0701619104, 1850020, 17426146.
27. Wade J, Camilla P, Coussens P, Tempelman RJ, Clayton DF, Lei L, Arnold AP, Agate R. A cDNA microarray from the telencephalon of juvenile male and female zebra finches. J Neurosci Methods 2004, 138:199-206. 10.1016/j.jneumeth.2004.04.007, 15325128.
28. Wada K, Howard JT, McConnell P, Whitney O, Lints T, Rivas MV, Horita H, Patterson MA, White SA, Scharff C, Haesler S, Zhao S, Sakaguchi H, Hagiwara M, Shiraki T, Hirozane-Kishikawa T, Skene P, Hayashizaki Y, Carninci P, Jarvis ED. A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc Natl Acad. Sci USA 2006, 103:15212-15217. 10.1073/pnas.0607098103, 1622802, 17018643.
29. Mukai M, Replogle K, Drnevich J, Wang G, Wacker D, Band M, Clayton DF, Wingfield JC. Seasonal differences of gene expression profiles in song sparrow (Melospiza melodia) hypothalamus in relation to territorial aggression. PLoS One 2009, 4:12:e8182. Mukai..
30. London SE, Dong S, Replogle K, Clayton DF. Developmental shifts in gene expression in the auditory forebrain during the sensitive period for song learning. Dev Neurobiol 2009, 69:437-450. 10.1002/dneu.20719, 2765821, 19360720.
31. R Development Core Team R: A language and environment for statistical computing 2010, Vienna, Austria: R Foundation for Statistical Computing, ISBN 3-900051-07-0, URL http://www.R-project.org/., R Development Core Team.
32. Smyth GK L. linear models for microarray data. Bioinformatics and Computational Biology Solutions using R and Bioconductor 2005, 397-420. New York: Springer, Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W.
33. Bioconductor Open software development for computational biology and bioinformatics Gentleman et al. Genome Biol 2004, Vol. 5:R80. www.bioconductor.org., Bioconductor.
34. Ritchie ME, Silver J, Oshlack A, Holmes M, Diyagama D, Holloway A, Smyth GK. A comparison of background correction methods for two-colour microarrays. Bioinformatics 2007, 23:2700-2707. 10.1093/bioinformatics/btm412, 17720982.
35. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods 2003, 31:265-273. 10.1016/S1046-2023(03)00155-5, 14597310.
36. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Statistical Society Series B 1995, 57:289-300.
37. Wu X, Watson M. M:CORNA: testing gene lists for regulation by microRNAs. Bioinformatics 2009, 25:832-833. 10.1093/bioinformatics/btp059, 2654799, 19181683.
38. Riters LV, Eens M, Pinxten R, Duffy DL, Balthazart J, Ball GF. Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm Behav 2000, 38:250-261. 10.1006/hbeh.2000.1623, 11104643.
39. Vicario DS. Organization of the zebra finch song control system: II. Functional organization of outputs from nucleus robustus archistriatalis. J Comp. Neurobiol. 1991, 2:63-73.
40. Margoliash D. Functional organization of forebrain pathways for song production and perception. J Neurobiol 1997, 33:671-693. 10.1002/(SICI)1097-4695(19971105)33:5<671::AID-NEU12>3.0.CO;2-C, 9369466.
41. Ball GF, Balthazart J. Neuroendocrine mechanisms regulating reproductive cycles and reproductive behavior in birds. Hormones, Brain and Behavior 2002, 649-798. San Diego: Academic Press, Pfaff DW.
42. Jarvis ED, Nottebohm F. Motor-driven gene expression. Proc Natl Acad Sci USA 1997, 94:4097-4102. 10.1073/pnas.94.8.4097, 20574, 9108111.
43. Stevenson TJ, Ball GF. information theory and the neuropeptidergic regulation of seasonal reproduction in mammals and birds. Proc Biol Sci Lond 2011, 278:2477-2485.
44. Ubuka T, Cadigan PA, Wang A, Liu J, Bentley GE. Identification of European starling GnRH1 precursor mRNA and its seasonal regulation. Gen Comp Endocrinol 2009, 162:301-306. 10.1016/j.ygcen.2009.04.001, 19362556.
45. Yamamura T, Hirunagi K, Ebihara S, Yoshimura T. Seasonal morphological changes in the neuro-glial interaction between gonadotropin-releasing hormone nerve terminals and glial endfeet in Japanese quail. Endocrinol 2004, 145:4264-4267.
46. Yoshimura T, Yasuo S, Watanbe M, Iigo M, Yamamura T, Hirunagi K, Ebihara S. Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 2003, 426:178-181. 10.1038/nature02117, 14614506.
47. Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K, Yasuo S, Katou Y, Kageyama S, Uno Y, Kasukawa T, Iigo M, Sharp PJ, Iwasawa A, Suzuki Y, Sugano S, Niimi T, Mizutani M, Namikawa T, Ebihara S, Ueda HR, Yoshimura T. Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 2008, 452:317-322. 10.1038/nature06738, 18354476.
48. Konishi M, Emlen ST, Ricklefs RE, Wingfield JC. Contributions of bird studies to biology. Science 1989, 246:465-472. 10.1126/science.2683069, 2683069.
49. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, Künstner A, Searle S, White S, Vilella AJ, Fairley S, Heger A, Kong L, Ponting CP, Jarvis ED, Mello CV, Minx P, Lovell P, Velho TA, Ferris M, Balakrishnan CN, Sinha S, Blatti C, London SE, Li Y, Lin YC, George J, Sweedler J, Southey B, Gunaratne P, Watson M, et al. The genome of a songbird. Nature 2010, 464:757-762. 10.1038/nature08819, 3187626, 20360741.