Testosterone and brain-derived neurotrophic factor interactions in the avian song control system

Neuroscience

Volumn 239, Issue , 2013, Pages 115-123

  Brenowitz, E A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

BDNF; Birdsong; Hormone; Plasticity; Song; Testosterone

Indexed keywords

ANDROSTANOLONE; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; ESTRADIOL; MESSENGER RNA; RECOMBINANT PROTEIN; TESTOSTERONE;

ANIMAL BEHAVIOR; BDNF GENE; BRAIN DEVELOPMENT; BRAIN REGION; BREEDING; CELL PROLIFERATION; CELL SURVIVAL; GENE; HIGH VOCAL CENTER; HORMONAL REGULATION; MOLECULAR INTERACTION; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; SEASONAL VARIATION; SEX DIFFERENCE; SONG CONTROL SYSTEM; SONGBIRD; TRKB GENE; VOICE;

ANIMALS; BIOLOGICAL EVOLUTION; BIRDS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; NEURONAL PLASTICITY; SEX CHARACTERISTICS; TESTOSTERONE; VOCALIZATION, ANIMAL;

EID: 84876085841     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.023     Document Type: Review

References (82)

1. Akutagawa E., Konishi M. Transient expression and transport of brain-derived neurotrophic factor in male zebra finch's song system during vocal development. Proc Natl Acad Sci U S A 1998, 95:11429-11434.
2. Alvarez-Borda B., Haripal B., Nottebohm F. Timing of brain-derived neurotrophic factor exposure affects life expectancy of new neurons. Proc Natl Acad Sci U S A 2004, 101:3957-3961.
3. Alvarez-Buylla A., Kirn J.R., Nottebohm F. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 1990, 249:1444-1446. [published erratum appears in Science 1990 Oct 19;250(4979):360].
4. Arnold A.P. Hormonally-induced alterations in synaptic organization in the adult nervous system. Exp Gerontol 1992, 27:99-110.
5. Ball G.F. Neuroendocrine basis of seasonal changes in vocal behavior among songbirds. Neural mechanisms of communication 2000, 213-253. MIT Press, Cambridge, MA. M. Hauser, M. Konishi (Eds.).
6. Ball G.F., Casto J.M., Bernard D.J. Sex differences in the volume of avian song control nuclei: comparative studies and the issue of brain nucleus delineation. Psychoneuroendocrinology 1994, 19:485-504.
7. Beecher M.D., Brenowitz E.A. Functional aspects of song learning in the songbirds. Trends Ecol Evol 2005, 20:143-149.
8. Bentley G.E., Brenowitz E.A. Three-dimensional analysis of avian song control nuclei. J Neurosci Methods 2002, 121:75-80.
9. Bothwell M. Functional interactions of neurotrophins and neurotrophin receptors. Annu Rev Neurosci 1995, 18:223-253.
10. Bottjer S.W., Glaessner S.L., Arnold A.P. Ontogeny of brain nuclei controlling song learning and behavior in zebra finches. J Neurosci 1985, 5:1556-1562.
11. Brainard M.S. The anterior forebrain pathway and vocal plasticity. Neuroscience of birdsong 2008, 240-255. Cambridge University Press, Cambridge. H.P. Zeigler, P. Marler (Eds.).
12. Brenowitz E.A. Comparative approaches to the avian song system. J Neurobiol 1997, 33:517-531.
13. Brenowitz E.A. Plasticity of the song control system in adult birds. Neuroscience of birdsong 2008, 332-349. Cambridge University Press, Cambridge. H.P. Zeigler, P. Marler (Eds.).
14. Brenowitz E.A., Arnold A.P. Interspecific comparisons of the size of neural song control regions and song complexity in duetting birds: evolutionary implications. J Neurosci 1986, 6:2875-2879.
15. Brenowitz E.A., Arnold A.P., Levin R.N. Neural correlates of female song in tropical duetting birds. Brain Res 1985, 343:104-112.
16. Brenowitz E.A., Beecher M.D. Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci 2005, 28:127-132.
17. Brenowitz E.A., Lent K. Afferent input is necessary for seasonal growth and maintenance of adult avian song control circuits. J Neurosci 2001, 21:2320-2329.
18. Brenowitz E.A., Lent K. Act locally and think globally: intracerebral testosterone implants induce seasonal-like growth of adult avian song control circuits. Proc Natl Acad Sci U S A 2002, 99:12421-12426.
19. Bridgham J.T., Carroll S.M., Thornton J.W. Evolution of hormone-receptor complexity by molecular exploitation. Science 2006, 312:97-101.
20. Catchpole C.K., Slater P.J.B. Bird song: biological themes and variations 2008, Cambridge University Press, Cambridge, UK.
21. Chen X., Agate R.J., Itoh Y., Arnold A.P. Sexually dimorphic expression of trkB, a Z-linked gene, in early posthatch zebra finch brain. Proc Natl Acad Sci U S A 2005, 102:7730-7735.
22. Dittrich F., Feng Y., Metzdorf R., Gahr M. Estrogen-inducible, sex-specific expression of brain-derived neurotrophic factor mRNA in a forebrain song control nucleus of the juvenile zebra finch. Proc Natl Acad Sci U S A 1999, 96:8241-8246.
23. Fraley G.S., Steiner R.A., Lent K., Brenowitz E.A. Seasonal changes in androgen receptor mRNA in the brain of the white-crowned sparrow. Gen Comp Endocrinol 2010, 166:66-71.
24. Gahr M., Metzdorf R. Distribution and dynamics in the expression of androgen and estrogen receptors in vocal control systems of songbirds. Brain Res Bull 1997, 44:509-517.
25. Gotz R., Raulf F., Schartl M. Brain-derived neurotrophic factor is more highly conserved in structure and function than nerve growth factor during vertebrate evolution. J Neurochem 1992, 59:432-442.
26. Hartog T.E., Dittrich F., Pieneman A.W., Jansen R.F., Frankl-Vilches C., Lessmann V., Lilliehook C., Goldman S.A., Gahr M. Brain-derived neurotrophic factor signaling in the HVC is required for testosterone-induced song of female canaries. J Neurosci 2009, 29:15511-15519.
27. Hidalgo A., Barami K., Iversen K., Goldman S.A. Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J Neurobiol 1995, 27:470-487.
28. Holloway C.C., Clayton D.F. Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nat Neurosci 2001, 4:170-175.
29. Jarvis E.D. Evolution of the pallium in birds and reptiles. New encyclopedia of neuroscience 2009, 1390-1400. Springer-Verlag GmbH, Berlin. M.D. Binder, N. Hirokawa, U. Windhorst (Eds.).
30. Johnson F., Hohmann S.E., DiStefano P.S., Bottjer S.W. Neurotrophins suppress apoptosis induced by deafferentation of an avian motor-cortical region. J Neurosci 1997, 17:2101-2111.
31. Knafo S., Esteban J.A. Common pathways for growth and for plasticity. Curr Opin Neurobiol 2012, 22:405-411.
32. Kohara K., Kitamura A., Morishima M., Tsumoto T. Activity-dependent transfer of brain-derived neurotrophic factor to postsynaptic neurons. Science 2001, 291:2419-2423.
33. Köhler H.-R., Kloas W., Schirling M., Lutz I., Reye A., Langen J.-S., Triebskorn R., Nagel R., Schönfelder G. Sex steroid receptor evolution and signalling in aquatic invertebrates. Ecotoxicology 2007, 16:131-143.
34. Levi-Montalcini R. The saga of the nerve growth factor. Neuroreport 1998, 9:R71-R83.
35. Louissaint A., Rao S., Leventhal C., Goldman S.A. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 2002, 34:945-960.
36. Luo M., Ding L., Perkel D.J. An avian basal ganglia pathway essential for vocal learning forms a closed topographic loop. J Neurosci 2001, 21:6836-6845.
37. MacDougall-Shackleton S.A., Ball G.F. Comparative studies of sex differences in the song-control system of songbirds. Trends Neurosci 1999, 22:432-436.
38. McCarthy M.M., Arnold A.P. Reframing sexual differentiation of the brain. Nat Neurosci 2011, 14:677-683.
39. Meitzen J., Moore I.T., Lent K., Brenowitz E.A., Perkel D.J. Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 2007, 27:12045-12057.
40. Meitzen J., Perkel D.J., Brenowitz E.A. Seasonal changes in intrinsic electrophysiological activity of song control neurons in wild song sparrows. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2007, 193:677-683.
41. Meitzen J., Weaver A.L., Brenowitz E.A., Perkel D.J. Plastic and stable electrophysiological properties of adult avian forebrain song-control neurons across changing breeding conditions. J Neurosci 2009, 29:6558-6567.
42. Moore I.T., Wingfield J.C., Brenowitz E.A. Plasticity of the avian song control system in response to localized environmental cues in an equatorial songbird. J Neurosci 2004, 24:10182-10185.
43. Murer M.G., Yan Q., Raisman-Vozari R. Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog Neurobiol 2001, 63:71-124.
44. Nottebohm F., Arnold A.P. Sexual dimorphism in vocal control areas of the songbird brain. Science 1976, 194:211-213.
45. Nottebohm F., Nottebohm M.E. Relationship between song repertoire and age in the canary Serinus canarius. Z Tierpsychol 1978, 46:298-305.
46. Nottebohm F., O'Loughlin B., Gould K., Yohay K., Alvarez-Buylla A. The life span of new neurons in a song control nucleus of the adult canary brain depends on time of year when these cells are born. Proc Natl Acad Sci U S A 1994, 91:7849-7853. [see comments].
47. ölveczky B.P., Andalman A.S., Fee M.S. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol 2005, 3:e153.
48. Park K.H., Meitzen J., Moore I.T., Brenowitz E.A., Perkel D.J. Seasonal-like plasticity of spontaneous firing rate in a songbird pre-motor nucleus. J Neurobiol 2005, 64:181-191.
49. Rasika S., Alvarez-Buylla A., Nottebohm F. BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain. Neuron 1999, 22:53-62.
50. Rasika S., Nottebohm F., Alvarez-Buylla A. Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc Natl Acad Sci U S A 1994, 91:7854-7858. [see comments].
51. Scharff C., Kirn J.R., Grossman M., Macklis J.D., Nottebohm F. Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron 2000, 25:481-492.
52. Scharfman H.E., Maclusky N.J. Similarities between actions of estrogen and BDNF in the hippocampus: coincidence or clue?. Trends Neurosci 2005, 28:79-85.
53. Scharfman H.E., MacLusky N.J. Estrogen and brain-derived neurotrophic factor (BDNF) in hippocampus: complexity of steroid hormone-growth factor interactions in the adult CNS. Front Neuroendocrinol 2006, 27:415-435.
54. Schlinger B., Brenowitz E.A. Neural and hormonal control of birdsong. Hormones, brain and behavior 2009, vol. 2:897-941. Academic Press, San Diego.
55. Schlinger B.A., Brenowitz E.A. Neural and hormonal control of birdsong. Hormones, brain and behavior 2002, vol. 2:799-839. Academic Press, New York.
56. Sehgal R.N., Lovette I.J. Molecular evolution of three avian neurotrophin genes: implications for proregion functional constraints. J Mol Evol 2003, 57:335-342.
57. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 2002, 25:507-536.
58. Smith G.T., Brenowitz E.A., Beecher M.D., Wingfield J.C. Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J Neurosci 1997, 17:6001-6010.
59. Smith G.T., Brenowitz E.A., Wingfield J.C. Roles of photoperiod and testosterone in seasonal plasticity of the avian song control system. J Neurobiol 1997, 32:426-442.
60. Soma K.K., Hartman V.N., Wingfield J.C., Brenowitz E.A. Seasonal changes in androgen receptor immunoreactivity in the song nucleus HVc of a wild bird. J Comp Neurol 1998, 409:224-236.
61. Soma K.K., Wissman A.M., Brenowitz E.A., Wingfield J.C. Dehydroepiandrosterone (DHEA) increases territorial song and the size of an associated brain region in a male songbird. Horm Behav 2002, 41:203-212.
62. Tettamanti G., Cattaneo A.G., Gornati R., de Eguileor M., Bernardini G., Binelli G. Phylogenesis of brain-derived neurotrophic factor (BDNF) in vertebrates. Gene 2010, 450:85-93.
63. Thompson C.K. Cell death and the song control system: a model for how sex steroid hormones regulate naturally-occurring neurodegeneration. Dev Growth Differ 2011, 53:213-224.
64. Thompson C.K., Bentley G.E., Brenowitz E.A. Rapid seasonal-like regression of the adult avian song control system. Proc Natl Acad Sci U S A 2007, 104:15520-15525.
65. Thompson C.K., Brenowitz E.A. Neurogenesis in an adult avian song nucleus is reduced by decreasing caspase-mediated apoptosis. J Neurosci 2009, 29:4586-4591.
66. Thompson C.K., Meitzen J., Replogle K., Drnevich J., Lent K.L., Wissman A.M., Farin F.M., Bammler T.K., Beyer R.P., Clayton D.F., Perkel D.J., Brenowitz E.A. Seasonal changes in patterns of gene expression in avian song control brain regions. PLoS ONE 2012, 7:e35119.
67. Thornton J.W. Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci U S A 2001, 98:5671-5676.
68. Tramontin A.D., Brenowitz E.A. A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning. J Neurobiol 1999, 40:316-326.
69. Tramontin A.D., Brenowitz E.A. Seasonal plasticity in the adult brain. Trends Neurosci 2000, 23:251-258.
70. Tramontin A.D., Hartman V.N., Brenowitz E.A. Breeding conditions induce rapid and sequential growth in adult avian song control circuits: a model of seasonal plasticity in the brain. J Neurosci 2000, 20:854-861.
71. Tramontin A.D., Perfito N., Wingfield J.C., Brenowitz E.A. Seasonal growth of song control nuclei precedes seasonal reproductive development in wild adult song sparrows. Gen Comp Endocrinol 2001, 122:1-9.
72. Tramontin A.D., Wingfield J.C., Brenowitz E.A. Androgens and estrogens induce seasonal-like growth of song nuclei in the adult songbird brain. J Neurobiol 2003, 57:130-140.
73. Tropea D., Van Wart A., Sur M. Molecular mechanisms of experience-dependent plasticity in visual cortex. Philos Trans R Soc B 2009, 364:341-355.
74. Trueta C., De-Miguel F.F. Extrasynaptic exocytosis and its mechanisms: a source of molecules mediating volume transmission in the nervous system. Front Physiol 2012, 3.
75. von Bartheld C.S., Byers M.R., Williams R., Bothwell M. Anterograde transport of neurotrophins and axodendritic transfer in the developing visual system. Nature 1996, 379:830-833.
76. Wade J. TrkB-like immunoreactivity in the song system of developing zebra finches. J Chem Neuroanat 2000, 19:33-39.
77. Wade J., Arnold A.P. Sexual differentiation of the zebra finch song system. Ann N Y Acad Sci 2004, 1016:540-559.
78. Wang Y., Brzozowska-Prechtl A., Karten H.J. Laminar and columnar auditory cortex in avian brain. Proc Natl Acad Sci U S A 2010, 107:12676-12681.
79. Wingfield J.C., Farner D.S. Environmental and endocrine control of seasonal reproduction in temperate zone birds. Prog Reprod Biol 1980, 5:62-101.
80. Wissman A.M., Brenowitz E.A. The role of neurotrophins in the seasonal-like growth of the avian song control system. J Neurosci 2009, 29:6461-6471.
81. Wray G.A., Levinton J.S., Shapiro L.H. Molecular evidence for deep precambrian divergences among metazoan phyla. Science 1996, 274:568-573.
82. Zeigler H.P., Marler P. Neuroscience of birdsong 2008, Cambridge University Press, Cambridge.