Song activation by testosterone is associated with an increased catecholaminergic innervation of the song control system in female canaries

Neuroscience

Volumn 121, Issue 3, 2003, Pages 801-814

  Appeltants, D ^a   Ball, G F ^b   Balthazart, J ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Analysis of variance; Androgen receptor; ANOVA; AR; Area ventralis of Tsai; AVT; CAergic; Catecholamine; Catecholaminergic; DA; DAergic; DLM; Dopamine; Dopaminergic; Dorsolateral thalamic nucleus; ER; Female canary; Learned vocalization; Songbird; Testosterone

Indexed keywords

TESTOSTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENDOCRINE SYSTEM; FEMALE; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; SONGBIRD; TELENCEPHALON; VARICOSIS; VISUAL SYSTEM;

ANIMALS; BEHAVIOR, ANIMAL; CANARIES; CATECHOLAMINES; CELL COUNT; FEMALE; IMMUNOHISTOCHEMISTRY; INFUSION PUMPS, IMPLANTABLE; NERVE FIBERS; SEX CHARACTERISTICS; SEXUAL MATURATION; TELENCEPHALON; TESTOSTERONE; TYROSINE 3-MONOOXYGENASE; VOCALIZATION, ANIMAL;

EID: 1342282577     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(03)00496-2     Document Type: Article

References (89)

1. Adler A., Vescovo P., Robionson J.K., Kritzer M.F. Gonadectomy in adult life increases tyrosine hydroxylase immunoreactivity in the prefrontal cortex and decrease open field activity in male rats. Neuroscience. 89:1999;939-954.
2. Appeltants D., Absil P., Balthazart J., Ball G.F. Identification of the origin of catecholaminergic inputs to HVC in canaries by retrograde tract tracing combined with tyrosine hydroxylase immunocytochemistry. J Chem Neuroanat. 18:2000;117-133.
3. Appeltants D., Ball G.F., Balthazart J. The distribution of tyrosine hydroxylase in the canary brain demonstration of a specific and sexually dimorphic catecholaminergic innervation of the telencephalic song control nuclei. Cell Tissue Res. 304:2001;237-259.
4. Appeltants D., Ball G.F., Balthazart J. The origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport. 13:2002;649-653.
5. Appeltants D., Del Negro C., Balthazart J. Noradrenergic control of auditory information processing in female canaries. Behav Brain Res. 133:2002;221-235.
6. Arnold A.P. The passerine bird song system as a model in neuroendocrine research. J Exp Zool. 4:1990;22-30.
7. Arnold A.P., Nottebohm F., Plaff D.W. Hormone concentrating cells in vocal control and other areas of the brain of the zebra finch (Poephila guttata). J Comp Neurol. 165:1976;487-511.
8. Bailhache T., Balthazart J. The catecholaminergic system of the quail brain immunocytochemical studies of dopamine β-hydroxylase and tyrosine hydroxylase. J Comp Neurol. 32:1993;230-256.
9. Ball G.F. Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars. Brain Behav Evol. 44:1994;234-246.
10. Ball G.F., Absil P., Balthazart J. Peptidergic delineations of nucleus interface reveal a sex difference in volume. Neuroreport. 6:1995;957-960.
11. Ball G.F., Hulse S.H. Bird song. Am Psychol. 53:1998;37-58.
12. Ball G.F. Neuroendocrine basis of seasonal changes in vocal behavior among songbirds. Hauser M., Konishi M. The design of animal communication. 1999;213-253 MIT Press, Cambridge, MA.
13. Ball G.F., Riters L.V., Balthazart J. Neuroendocrinology of song behavior and avian brain plasticity multiple sites of action of sex steroid hormones. Front Neuroendocrinol. 23:2002;137-178.
14. Balthazart J., Foidart A., Wilson E.M., Ball G.F. Immunocytochemical localization of androgen receptors in the male song bird and quail brain. J Comp Neurol. 17:1992;407-420.
15. Balthazart J., Ball G.F. Sexual differentiation of brain and behavior in birds. Trend Endocrinol Metab. 6:1995;21-29.
16. Barclay S.R., Harding C.F. Androstenedione modulation of monoamine levels and turnover in hypothalamic and vocal control nuclei in the male zebra finch steroid effects on brain monoamines. Brain Res. 459:1988;333-343.
17. Barclay S.R., Harding C.F. Differential modulation of monoamines levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches. Brain Res. 523:1990;251-262.
18. Barclay S.R., Harding C.F., Waterman S.A. Correlation between catecholamines levels and sexual behavior in male zebra finches. Pharmacol Biochem Behav. 41:1992;195-201.
19. Barclay S.R., Harding C.F., Waterman S.A. Central DSP-4 treatment decreases norepinephrine levels and courtship behavior in male zebra finches. Pharmacol Biochem Behav. 53:1996;213-220.
20. Bernard D.J., Ball G.F. Two histological markers reveal a similar photoperiodic differences in the volume of the high vocal center in male European starling. J Comp Neurol. 360:1995;726-734.
21. Bernard D.J., Bentley G.E., Balthazart J., Turek F.W., Ball G.F. Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starling. Endocrinology. 140:1999;4633-4643.
22. Benton S., Nelson D.A., Marler P., DeVoogd T.J. Anterior forebrain pathway is needed for stable song expression in adult white-crowned sparrows (Zonotrichia leucophrys). Behav Brain Res. 96:1998;135-150.
23. Beyer C., Feder H.H. Sex steroids and afferent input their roles in brain sexual differentiation. Annu Rev Physiol. 49:1987;349-364.
24. Bottjer S.W., Schoonmaker J.N., Arnold A.P. Auditory and hormonal stimulation interact to produce neural growth in adult canaries. J Neurobiol. 17:1986;605-612.
25. Bottjer S.W., Dignan T.P. Joint hormonal and sensory stimulation modulate neuronal number in adult canary brains. J Neurobiol. 19:1988;624-635.
26. Bottjer S.W., Maier E. Testosterone and the incidence of hormone target cells in song-control nuclei of adult canaries. J Neurobiol. 22:1991;512-521.
27. Bottjer S.W. The distribution of tyrosine hydroxylase in the brains of male and female zebra finches. J Neurobiol. 24:1993;51-69.
28. Bottjer S.W., Roselinsky H., Tran N.B. Sex differences in neuropeptide staining of song-control nuclei in zebra finch brains. Brain Behav Evol. 50:1997;284-303.
29. Bottjer S.W., Johnson F. Circuits, hormones, and learning vocal behavior in songbirds. J Neurobiol. 33:1997;602-618.
30. Brenowitz E.A., Arnold A.P. The effects of systemic androgen treatment on androgen accumulation in song control regions of the adult female canary brain. J Neurobiol. 21:1990;837-843.
31. Brenowitz E.A., Margoliash D., Nordeen K. An introduction to birdsong and the avian song system. J Neurobiol. 33:1997;495-500.
32. Brozoski T.J., Brown R.M., Rosvold H.E., Goldman P.S. Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science. 205:1979;929-932.
33. Canady R.A., Burd G.D., DeVoogd T.J., Nottebohm F. Effect of testosterone on input received by an identified neuron type of the canary song system a Golgi/electron microscopy/degeneration study. J Neurosci. 8:1988;3770-3784.
34. Casto J.M., Ball G.F. Characterization and localization of D1 dopamine receptors in the sexually dimorphic vocal control nucleus, area X, and the basal ganglia of European starlings. J Neurobiol. 25:1994;767-780.
35. Dave A.S., Yu A.C., Margoliash D. Behavioral state modulation of auditory activity in a vocal motor system. Science. 282:1998;2250-2254.
36. DeVoogd T.J., Nottebohm F. Sex differences in dendritic morphology of a song control nucleus in the canary a quantitative Golgi-study. J Comp Neurol. 196:1981;309-316.
37. DeVoogd T.J., Nottebohm F. Gonadal hormones induce dendritic growth in the adult brain. Science. 214:1981;202-204.
38. DeVoogd T.J., Nixdorf B., Nottebohm F. Synaptogenesis and changes in synaptic morphology related to acquisitive new behavior. Brain Res. 329:1985;304-308.
39. Ding L., Perkel D.J. Dopamine modulates excitability of spiny neurons in the avian basal ganglia. J Neurosci. 22:2002;5210-5218.
40. Doupe A.J., Solis M.M. Song- and order-selective neurons develop in the songbird anterior forebrain during vocal learning. J Neurobiol. 33:1997;694-709.
41. Doupe A.J., Brainard M.S., Hessler N.A. The song system: neural circuits essential throughout life for vocal behavior and plasticity. Gazzaniga M.S. The new cognitive neurosciences. 2nd ed:2000;451-467 MIT Press, Cambridge, MA.
42. Doupe A.J., Kuhl P.K. Birdsong and human speech common themes and mechanisms. Annu Rev Neurosci. 22:1999;567-631.
43. Durstewitz D., Kröner S., Güntürkün O. The dopaminergic innervation of the avian telencephalon. Prog Neurobiol. 59:1999;161-195.
44. Durstewitz D., Seamans J.K., Sejnowski T.J. Neurocomputational models of working memory. Nat Neurosci. 3:(Suppl):2000;1184-1191.
45. Durstewitz D., Seamans J.K., Sejnowski T.J. Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. J Neurophysiol. 83:2000;1733-1750.
46. Dutar P., Vu H.M., Perkel D.J. Multiple cell types distinguished by physiological, pharmacological, and anatomical properties in nucleus HVC of the adult zebra finch. J Neurophysiol. 80:1998;1828-1838.
47. Etgen A.M., Vathy I., Petitti N., Ungar S., Karkanias G.B. Ovarian steroids, female reproductive behavior and norepinephrine neurotransmission in the hypothalamus. Balthazart J. Hormone, brain and behaviour in vertebrates, 2: behavioural activation in males and females: social interactions and reprodutive physiology: comparative physiology, Vol. 9s. 1990;116-128 Karger, Basel.
48. Etgen A.M., Ungar S., Petitti N. Estradiol and progesterone modulation of norepinephrine neurotransmission implications for the regulation of female reproductive behavior. J Neuroendocrinol. 4:1992;255-271.
49. Flor-Henry P. Influence of gender in schizophrenia as related to other psychopathological syndromes. Schizophr Bull. 16:1990;211-228.
50. Foster E.F., Mehta R.P., Bottjer S.W. Axonal connections of the medial magnocellular nucleus of the anterior neostriatum in zebra finches. J Comp Neurol. 382:1997;364-381.
51. Gahr M., Guttinger H.R., Kroodsma D.E. Estrogen receptors in the avian brain survey reveals general distribution and forebrain areas unique to songbirds. J Comp Neurol. 327:1993;112-122.
52. Gahr M., Garcia-Segura L.M. Testosterone-dependent increase of gap-junctions in HVC neurons of adult female canaries. Brain Res. 712:1996;69-73.
53. Gulledge C.C., Deviche P. Age- and sex-related differences in opioid receptor densities in the songbird vocal control system. J Comp Neurol. 404:1999;505-514.
54. Hampson E. Variations in sex related cognitive abilities across the menstrual cycle. Brain Cogn. 14:1990;26-43.
55. Hampson E., Kimura D. Sex differences and hormonal influences on cognitive function in humans. Becker J.B., Breedlove S.M., Crews D. Behavioral endocrinology. 1992;357-398 MIT Press, Cambridge, MA.
56. Kelly S.J., Ostrowski N.L., Wilson M.A. Gender differences in brain and behavior hormonal and neural bases. Pharmacol Biochem Behav. 64:1999;655-664.
57. Kimura D., Hampson E. Cognitive pattern in men and women is influenced by fluctuation in sex hormones. Curr Directions Psychol Sci. 3:1994;57-61.
58. Kritzer M.F., Kohama S.G. Ovarian hormones influence the morphology, distribution, and density of tyrosine hydroxylase immunoreactive axons in the dorsolateral prefrontal cortex of adult rhesus monkeys. J Comp Neurol. 395:1998;1-17.
59. Leitner S., Voigt C., Garcia-Segura L.M., Van't Hof T., Gahr M. Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas. Horm Behav. 40:2001;160-168.
60. Lewis J.W., Ryan S.M., Arnold A.P., Butcher L.L. Evidence for catecholamine projection to area X in the zebra finch. J Comp Neurol. 196:1981;347-354.
61. Maney D.L., Bernard D.J., Ball G.F. Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem. Neurosci Lett. 311:2001;189-192.
62. Margoliash D. Functional organization of forebrain pathways for song production and perception. J Neurobiol. 33:1997;671-693.
63. McNeil T.F., Kaij L., Malmquist-Larsson A. Woman with non-organic psychosis pregnancy's effect on mental health during pregnancy. Acta Psychiatr Scand. 70:1984;140-148.
64. Mello C.V., Pinaud R., Ribeiro S. Noradrenergic system of the zebra finch brain immunocytochemical study of dopamine-β-hydroxylase. J Comp Neurol. 400:1998;207-228.
65. Nastiuk K.L., Clayton D.F. The canary androgen receptor mRNA is localized in the song control nuclei in the brain and is rapidly regulated by testosterone. J Neurobiol. 26:1995;213-224.
66. Nicholls T.J., Goldsmith A.R., Dawson A. Photorefractoriness in birds and comparison with mammals. Physiol Rev. 68:1988;133-176.
67. Nock B., Feder H.H. Neurotransmitter modulation of steroid action in target cells that mediate reproduction and reproductive behavior. Neurosci Biobehav Rev. 5:1981;. 537-447.
68. Nottebohm F., Arnold A.P. Sexual dimorphism in the vocal control areas in song bird brain. Science. 194:1976;211-213.
69. Nottebohm F. Testosterone triggers growth of brain vocal control nuclei in adult female canaries. Brain Res. 189:1980;429-436.
70. Nottebohm F., Kelley D.B., Paton J.A. Connections of vocal control nuclei in the canary telencephalon. J Comp Neurol. 207:1982;344-357.
71. Nottebohm F., Nottebohm M.E., Crane L.A., Wingfield J.C. Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. Behav Neural Biol. 47:1987;197-211.
72. Nottebohm F. The anatomy and timing of vocal learning in birds. Hauser M.D., Konishi M. The design of animal communication. 1999;63-110 MIT Press, Cambridge, MA.
73. Pasqualini C., Olivier V., Guibert B., Frain O., Leviel V. Acute stimulatory effect of estradiol on striatal dopamine synthesis. J Neurochem. 65:1995;1651-1657.
74. Pesch A., Güttinger H.R. Der Gesang des weiblichen Kanarienvogels. J Ornithol. 126:1985;108-110.
75. Rasika S., Alvarez-Buylla A., Nottebohm F. BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain. Neuron. 22:1999;53-62.
76. Reiner A., Karle E.J., Anderson K.D., Medina L. Catecholaminergic perikarya and fibers in the avian nervous system. Smeets W.J.A.J., Reiner A. Phylogeny and development of catecholamine systems in the CNS of vertebrates. 1994;135-181 Cambridge University Press, Cambridge.
77. Reznikov A.G., Nosenko N.D. It is possible that noradrenaline is the biogenic monoamine responsible for androgen-dependent sexual brain differentiation. Exp Clin Endocrinol. 81:1983;91-93.
78. Reznikov A.G., Nosenko N.D. Catecholamines in steroid-dependent brain development. J Steroid Biochem Mol Biol. 53:1995;349-353.
79. Riters L.V., Ball G.F. Sex differences in the densities of alpha 2-adrenergic receptors in the song control system, but not the medial preoptic nucleus in zebra finches. J Chem Neuroanat. 23:2002;269-277.
80. Sakaguchi H., Saito N. The acetylcholine and catecholamine contents in song control nuclei of zebra finch during song ontogeny. Dev Brain Res. 47:1989;313-317.
81. Sawaguchi T., Goldman-Rakic P.S. D1 dopamine receptors in prefrontal cortex involvement in working memory. Science. 251:1991;947-950.
82. Schlinger B.A. Sex steroids and their actions on the birdsong system. J Neurobiol. 33:1997;619-631.
83. Seeman M.V., Lang M. The role of estrogens in schizophrenia gender differences. Schizophr Bull. 16:1990;185-191.
84. Siddiqui A., Gilmore D.P. Regional differences in the catecholamine content of the rat brain effects of neonatal castration and androgenization. Acta Endocrinol (Copenh). 118:1988;483-494.
85. Soha J.A., Shimizu T., Doupe A.J. Development of the catecholaminergic innervation of the song system of the male zebra finch. J Neurobiol. 29:1996;473-489.
86. Stokes T.M., Leonard C.M., Nottebohm F. The telencephalon, diencephalon, and mesencephalon of the canary, Sirinus canaria, in stereotaxic coordinates. J Comp Neurol. 156:1974;337-374.
87. Troyer T.W., Bottjer S.W. Birdsong models and mechanisms. Curr Opin Neurobiol. 11:2001;721-726.
88. Weiler R., Pottek M., He S., Vaney D.I. Modulation of coupling between retinal horizontal cells by retinoic acid and endogenous dopamine. Brain Res Rev. 32:2000;121-129.
89. Wild J.M. Neural pathways for the control of birdsong production. J Neurobiol. 33:1997;653-670.