estradiol; norepinephrine; song learning; seasonal reproduction; zebra finch; European starling
Abstract :
[en] Birdsong is a species-typical stereotypic vocalization produced in the context of reproduction and aggression. Among temperate-zone songbirds, it is produced primarily by males, and its frequency and quality are enhanced by the presence of the gonadal steroid hormone testosterone in the plasma. In the brain, the effects of testosterone on song behavior involve both estrogenic and androgenic metabolites of testosterone that are locally produced and act via their cognate receptors. Androgen, and in some cases estrogen, receptors are present in many specialized forebrain song control nuclei. Testosterone can regulate catecholamine steady-state levels and turnover in these song control regions. Tracing studies combined with immunocytochemistry for tyrosine hydroxylase (a marker of catecholamine synthesis) reveal several catecholamine cell groups that project to forebrain song control nuclei. These brain areas also express the mRNA for either androgen receptors or estrogen receptor alpha, and androgens enhance the expression of tyrosine hydroxylase. Dopaminergic cell groups that project to song nuclei express the protein product of the immediate early gene fos in association with the production of territorial song. Thus, testosterone may be acting on song behavior via these ascending catecholamine cell groups. Chemical lesioning studies suggest that noradrenergic projections to the song system are involved in the latency to produce song and the ability to discriminate conspecific from heterospecific song. The song control circuit may thus be modulated in significant ways via the androgen regulation of forebrain catecholamine systems.
Disciplines :
Neurosciences & behavior
Author, co-author :
Ball, G. F.
Castelino, C. B.
Maney, D. L.
Appeltants, D.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Language :
English
Title :
The activation of birdsong by testosterone - Multiple sites of action and role of ascending catecholamine projections
Publication date :
2003
Journal title :
Annals of the New York Academy of Sciences
ISSN :
0077-8923
eISSN :
1749-6632
Publisher :
New York Acad Sciences, New York, United States - New York
Becker, J.B., Breedlove, S.M., Introduction to behavioral endocrinology (2002) Behavioral Endocrinology, pp. 3-38. , J.B. Becker, S.M. Breedlove, D. Crews & M.M. McCarthy, Eds.: MIT Press. Cambridge, MA
Silver, R., The parental behavior of ring doves (1978) Am. Scientist, 66, pp. 209-215
Barfield, R.J., Activation of copulatory behavior by androgen implanted into the preoptic area of the male fowl (1969) Horm. Behav., 1, pp. 37-52
Lisk, R.D., Diencephalic placement of estradiol and sexual receptivity in the female rat (1962) Am. J. Physiol., 203, pp. 493-496
Lisk, R.D., Neural localization for androgen activation of copulatory behavior in the male rat (1967) Endocrinology, 80, pp. 754-761
Hull, E.M., Meisel, R.L., Sachs, B.D., Male sexual behavior (2002) Hormones, Brain, and Behavior, 2, pp. 1-137. , D.W. Pfaff, A.P. Arnold, A.M. Etgen, et al., Eds.: Academic Press. San Diego, CA
Blaustein, J.D., Erskine, M.S., Feminine sexual behavior: Cellular integration of hormonal and afferent information in the rodent brain (2002) Hormones, Brain, and Behavior, 1, pp. 139-214. , D.W. Pfaff, A.P. Arnold, A.M. Etgen, et al., Eds.: Academic Press. San Diego, CA
Pfaff, D.W., Ogawa, S., Kia, K., Genetic mechansims in neural and hormonal controls over female reproductive behaviors (2002) Hormones, Brain, and Behavior, 3, pp. 441-510. , D.W. Pfaff, A.P. Arnold, A.M. Etgen, et al., Eds.: Academic Press. San Diego, CA
Etgen, A.M., Estrogen regulation of neurotransmitter and growth factor signaling in the brain (2002) Hormones, Brain, and Behavior, 3, pp. 381-440. , D.W. Pfaff, A.P. Arnold, A.M. Etgen, et al., Eds. Academic Press. San Diego
Larsson, K., Heimer, L., Mating behaviour of male rats after lesions in the preoptic area (1964) Nature, 202, pp. 413-414
Heimer, L., Larsson, K., Impairment of mating behavior in male rats following lesions in the preoptic-anterior hypothalamic continuum (1966) Brain Res., 3, pp. 248-263
Dominguez, J., Riolo, J.V., Xu, Z.J., Hull, E.M., Regulation by the medial amygdala of copulation and medial preoptic dopamine release (2001) J. Neurosci., 21, pp. 349-355
Calizo, L.H., Flanagan-Cato, L.M., Estrogen-induced dendritic spine elimination on female rat ventromedial hypothalamic neurons that project to the periaqueductal gray (2002) J. Comp. Neurol., 447, pp. 234-248
Catchpole, C.K., Slater, P.J.B., (1995) Bird Song: Biological Themes and Variations. 1st Edit., , Cambridge University Press. New York
Brenowitz, E.A., Comparative approaches to the avian song system (1997) J. Neurobiol., 33, pp. 517-531
Ball, G.F., Hulse, S.H., Bird song (1998) Am. Psychol., 53, pp. 37-58
Ball, G.F., Riters, L.V., Balthazart, J., Neuroendocrinology of song behavior and avian brain plasticity: Multiple sites of action of sex steroid hormones (2002) Front. Neuroendocrinol., 23, pp. 137-178
Schlinger, B.A., Brenowitz, E.A., Neural and hormonal control of birdsong (2002) Hormones, Brain, and Behavior, 2, pp. 799-839. , D.W. Pfaff, A.P. Arnold, A.M. Etgen, et al., Eds.: Academic Press. San Diego
Arnold, A.P., Nottebohm, F., Pfaff, D.W., Hormone concentrating cells in vocal control areas of the brain of the zebra finch (Poephila guttata) (1976) J. Comp. Neurol., 165, pp. 487-512
Balthazart, J., Foidart, A., Wilson, E.M., Ball, G.F., Immunocytochemical localization of androgen receptors in the male songbird and quail brain (1992) J. Comp. Neurol., 317, pp. 407-420
Gahr, M., Güttinger, H.-R., Kroodsma, D.E., Estrogen receptors in the avian brain: Survey reveals general distribution and forebrain areas unique to songbirds (1993) J. Comp. Neurol., 327, pp. 112-122
Bernard, D.J., Bentley, G.E., Balthazart, J., Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings (1999) Endocrinology, 140, pp. 4633-4643
Metzdorf, R., Gahr, M., Fusani, L., Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds (1999) J. Comp. Neurol., 407, pp. 115-129
Arnold, A.P., The passerine bird song system as a model in neuroendocrine research (1990) J. Exp. Zool., 4, pp. 22-30
Doupe, A.J., Kuhl, P.K., Birdsong and human speech: Common themes and mechanisms (1999) Annu. Rev. Neurosci., 22, pp. 567-631
Alvarez-Borda, B., Nottebohm, F., Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain (2002) J. Neurosci., 22, pp. 8684-8690
Margoliash, D., Functional organization of forebrain pathways for song production and perception (1997) J. Neurobiol., 33, pp. 671-693
Wild, J.M., Neural pathways for the control of birdsong production (1997) J. Neurobiol., 33, pp. 653-670
Brenowitz, E.A., Margoliash, D., Nordeen, K.W., An introduction to birdsong and the avian song system (1997) J. Neurobiol., 33, pp. 495-500
Nottebohm, F., Brain pathways for vocal learning in birds: A review of the first 10 years (1980) Progress in Psychobiology and Physiological Psychology, 9, pp. 85-214. , J.M. Sprague & A.N. Epstein, Eds.: Academic Press. New York
Nottebohm, F., The search for neural mechanisms that define the sensitive period for song learning in birds (1993) Neth. J. Zool., 43, pp. 193-234
Nottebohm, F., Stokes, T.M., Leonard, C.M., Central control of song in the canary, Serinus canarius (1976) J. Comp. Neurol., 165, pp. 457-486
Simpson, H.B., Vicario, D.S., Brain pathways for learned and unlearned vocalizations differ in zebra finches (1990) J. Neurosci., 10, pp. 1541-1556
Jarvis, E.D., Nottebohm, F., Motor-driven gene expression (1997) Proc. Natl. Acad. Sci. USA, 94, pp. 4097-4102
Kimpo, R.R., Doupe, A.J., FOS is induced by singing in distinct neuronal populations in a motor network (1997) Neuron, 18, pp. 315-325
Yu, A.C., Margoliash, D., Temporal hierarchical control of singing in birds (1996) Science, 273, pp. 1871-1875
Bottjer, S.W., Johnson, F., Circuits, hormones, and learning: Vocal behavior in songbirds (1997) J. Neurobiol., 33, pp. 602-618
Benton, S., Nelson, D.A., Marler, P., Devoogd, T.J., Anterior forebrain pathway is needed for stable song expression in adult male white-crowned sparrows (Zonotrichia leucophrys) (1998) Behav. Brain Res., 96, pp. 135-150
Bottjer, S.W., Miesner, E.A., Arnold, A.P., Forebrain lesions disrupt development but not maintenance of song in passerine birds (1984) Science, 224, pp. 901-903
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 (1991) J. Neurosci., 11, pp. 2896-2913
Sohrabji, F., Nordeen, E.J., Nordeen, K.W., Selective impairment of song learning following lesions of a forebrain nucleus in juvenile zebra finches (1990) Behav. Neural Biol., 53, pp. 51-63
Ball, G.F., Neuroendocrine basis of seasonal changes in vocal behavior among songbirds (1999) The Design of Animal Communication, pp. 213-253. , M. Hauser & M. Konishi, Eds.: MIT Press. Cambridge, MA
Wingfield, J.C., Farner, D.S., Endocrinology of reproduction in wild species (1993) Avian Biology, 9, pp. 163-327. , D.S. Farner, J. King & K.C. Parkes, Eds: Vol. 9. Academic Press. New York
Dawson, A., King, V.M., Bentley, G.E., Ball, G.F., Photoperiodic control of seasonality in birds (2001) J. Biol. Rhythms, 16, pp. 365-380
Balthazart, J., Hormonal correlates of behavior (1983) Avian Biology, 7, pp. 221-365. , D.S. Farner, J. R. King, K. C. Parkes, Eds.: Academic Press. New York
Pröve, E., Der Einfluss von Kastration und Testosteronsubstitution auf das Verhalten manlicher Zebrafinken (1974) J. Ornithol., 115, pp. 338-347
Arnold, A.P., The effects of castration and androgen replacement on song courtship, and aggression in zebra finches (1975) J. Exp. Zool., 191, pp. 309-326
Wingfield, J.C., Hahn, T.P., Testosterone and territorial behaviour in sedentary and migratory sparrows (1994) Anim. Behav., 47, pp. 77-89
Eens, M., Understanding the complex song of the European starling: An integrated ethological approach (1997) Adv. Study Anim. Behav., 26, pp. 355-434
Riters, L.V., Eens, M., Pinxten, R., Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris) (2000) Horm. Behav., 38, pp. 250-261
De Ridder, E., Pinxten, R., Eens, M., Experimental evidence of a testosterone-induced shift from paternal to mating behaviour in a facultatively polygynous songbird (2000) Behav. Ecol. Sociobiol., 49, pp. 24-30
Pinxten, R., De Ridder, E., Balthazart, J., Eens, M., Context-dependent effects of castration and testosterone treatment on song in male European starlings. Horm (2002) Behav., 42, pp. 307-318
Adkins-Regan, E., Hormone specificity, androgen metabolism, and social behavior (1981) Am. Zool., 21, pp. 257-271
Adkins-Regan, E., Sex steroids and the differentiation and activation of avian reproductive behaviour (1983) Hormones and Behaviour in Higher Vertebrates, pp. 219-228. , J. Balthazart & R. Gilles, Eds.: Springer-Verlag. Berlin
Balthazart, J., Steroid metabolism and the activation of social behavior (1989) Advances in Comparative and Environmental Physiology, 1st Edit., 3, pp. 105-159. , J. Balthazart, Ed.: Springer Verlag. Berlin
Hutchison, J.B., A role for brain metabolism in the behavioural action of androgen (1987) Highlights on Endocrinology Bogtrykkeri, pp. 429-436. , C. Christiansen & B.J. Riis, Eds.: Copenhagen
Balthazart, J., Tlemçani, O., Ball, G.F., Do sex differences in the brain explain sex differences in the hormonal induction of reproductive behavior? What 25 years of research on the Japanese quail tells us (1996) Horm. Behav., 30, pp. 627-661
Schlinger, B.A., Sex steroids and their actions on the birdsong system (1997) J.Neurobiol., 33, pp. 619-631
Ball, G.F., Balthazart, J., Neuroendocrine mechanisms regulating reproductve cycles and reproductive behavior in birds (2002) Hormones, Brain, and Behavior, 2, pp. 649-798. , D. W. Pfaff, A.P. Arnold, A.M. Etgen, et al., Eds.: Academic Press. San Diego
Harding, C.F., Sheridan, K., Walters, M.J., Hormonal specificity and activation of sexual behavior in male zebra finches (1983) Horm. Behav., 17, pp. 111-133
Walters, M.J., Harding, C.F., The effects of an aromatization inhibitor on the reproductive behavior of male zebra finches (1988) Horm. Behav., 22, pp. 207-218
Harding, C.F., Walters, M.J., Collado, D., Sheridan, K., Hormonal specificity and activation of social behavior in male red-winged blackbirds (1988) Horm. Behav., 22, pp. 402-418
Fusani, L., Metzdorf, R., Hutchison, J.B., Gahr, M., Aromatase inhibition affects testosterone-induced masculinization of song and the neural song system in female canaries (2003) J. Neurobiol., 54, pp. 370-379
Kelley, D.B., Pfaff, D.W., Generalizations from comparative studies on neuroanatomical and endocrine mechanisms of sexual behaviour (1978) Biological Determinants of Sexual Behaviour, pp. 225-254. , J.B. Hutchison, Ed.: John Wiley & Sons. Chichester
Morrell, J.I., Pfaff, D.W., A neuroendocrine approach to brain function: Localization of sex steroid concentrating cells in vertebrate brains (1978) Am. Zool., 18, pp. 447-460
Ball, G.F., Chemical neuroanatomical studies of the steroid-sensitive songbird vocal control system: A comparative approach (1990) Hormones, Brain, and Behaviour in Vertebrates. Vol. 8: Sexual Differentiation, Neuroanatomical Aspects, Neurotransmitters, and Neuropeptides, 8, pp. 148-167. , J. Balthazart, Ed.: Karger. Basel
Brenowitz, E.A., Evolution of the vocal control system in the avian brain (1991) Semin. Neurosci., 3, pp. 399-407
Morrell, J.I., Kelley, D.B., Pfaff, D.W., Sex steroid binding in the brain of vertebrates (1975) Brain-Endocrine Interactions II, pp. 230-256. , K.M. Knigge, D.E. Scott, H. Kobayashi, et al., Eds.: Karger. Basel
Pfaff, D.W., The neuroanatomy of sex hormone receptors in the vertebrate brain (1976) Neuroendocrine Regulation of Fertility, pp. 30-45. , T.C. Anand Kumar, Ed.: Karger. Basel
Stumpf, W.E., Sar, M., Anatomical distribution of estrogen, androgen, progestin, corticoid and thyroid hormone target sites in the brain of mammals: Phylogeny and ontogeny (1978) Am. Zool., 18, pp. 435-445
Konishi, M., Birdsong: From behavior to neuron (1985) Annu. Rev. Neurosci., 8, pp. 125-170
Nottebohm, F., Arnold, A.P., Sexual dimorphism in the vocal control areas in the song bird brain (1976) Science, 194, pp. 211-213
Nottebohm, F., Alvarez-Buylla, A., Cynx, J., Song learning in birds: The relation between perception and production (1990) Philos. Trans. R. Soc. Lond. [Biol.], 329, pp. 115-124
Gahr, M., Localization of androgen receptors and estrogen receptors in the same cells of the songbird brain (1990) Proc. Natl. Acad. Sci. USA, 87, pp. 9445-9448
Lücke, J., Haase, E., Autoradiographische Untersuchungen am Gehirn von Bergfinken (Fringilla montifringilla L.) nach injektion von 3H-Testosteron (1980) J. Hirnforsch., 21, pp. 369-380
Zigmond, R.E., Nottebohm, F., Pfaff, D.W., Androgen-concentrating cells in the midbrain of a songbird (1973) Science, 179, pp. 1005-1007
Harding, C.F., Walters, M.J., Parsons, B., Androgen receptor levels in hypothalamic and vocal control nuclei in the male zebra finch (1984) Brain Res., 306, pp. 333-339
Arnold, A.P., Saltiel, A., Sexual difference in pattern of hormone accumulation in the brain of a song bird (1979) Science, 205, pp. 702-705
Nordeen, E.J., Nordeen, K.W., Arnold, A.P., Sexual differentiation of androgen accumulation within the zebra finch brain through selective cell loss and addition (1987) J. Comp. Neurol., 259, pp. 393-399
Sohrabji, F., Nordeen, K.W., Nordeen, E.J., Projections of androgen-accumulating neurons in a nucleus controlling avian song (1989) Brain Res., 488, pp. 253-259
Smith, G.T., Brenowitz, E.A., Prins, G.S., Use of PG-21 immunocytochemistry to detect androgen receptors in the songbird brain (1996) J. Histochem. Cytochem., 44, pp. 1075-1080
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 (1999) J. Comp. Neurol., 409, pp. 224-236
Nastiuk, K.L., Clayton, D.F., Seasonal and tissue-specific regulation of canary androgen receptor messenger ribonucleic acid (1994) Endocrinology, 134, pp. 640-649
Gahr, M., Metzdorf, R., Distribution and dynamics in the expression of androgen and estrogen receptors in vocal control systems of songbirds (1997) Brain Res. Bull., 44, pp. 509-517
Fusani, L., Van't Hof, T., Hutchison, J.B., Gahr, M., Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens (2000) J. Neurobiol., 43, pp. 254-268
Nastiuk, K.L., Clayton, D.F., The canary androgen receptor mRNA is localized in the song control nuclei of the brain and is rapidly regulated by testosterone (1995) J. Neurobiol., 26, pp. 213-224
Maney, D.L., Bernard, D.J., Ball, G.F., Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem (2001) Neurosci. Lett., 311, pp. 189-192
Nordeen, K.W., Nordeen, E.J., Arnold, A.P., Estrogen establishes sex differences in androgen accumulation in zebra finch brain (1986) J. Neurosci., 6, pp. 734-738
Bottjer, S.W., Halsema, K.A., Brown, S.A., Miesner, E.A., Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches (1989) J. Comp. Neurol., 279, pp. 312-326
Ball, G.F., Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars (1994) Brain Behav. Evol., 44, pp. 234-246
Reinke, H., Wild, J.M., Identification and connections of inspiratory premotor neurons in songbirds and budgerigar (1998) J. Comp. Neurol., 391, pp. 147-163
Wild, J.M., Li, D.F., Eagleton, C., Projections of the dorsomedial nucleus of the intercollicular complex (DM) in relation to respiratory-vocal nuclei in the brain-stem of pigeon (Columba livia) and zebra finch (Taeniopygia guttata) (1997) J. Comp. Neurol., 377, pp. 392-413
Gahr, M., Wild, J.M., Localization of androgen receptor mRNA-containing cells in avian respiratory-vocal nuclei: An in situ hybridization study (1997) J. Neurobiol., 33, pp. 865-876
Gahr, M., Neural song control system of hummingbirds: Comparison to swifts, vocal learning (songbirds) and nonlearning (suboscines) passerines, and vocal learning (budgerigars) and nonlearning (dove, owl, gull, quail, chicken) nonpasserines (2000) J. Comp. Neurol., 426, pp. 182-196
Kuiper, G.G.J.M., Enmark, E., Pelto-Huikko, M., Cloning of a novel estrogen receptor expressed in rat prostate and ovary (1996) Proc. Natl. Acad. Sci. USA, 93, pp. 5925-5930
Mosselman, S., Polman, J., Dijkema, R., ER beta: Identification and characterization of a novel human estrogen receptor (1996) FEBS Lett., 392, pp. 49-53
Tremblay, G.B., Tremblay, A., Copeland, N.G., Cloning, chromosomal localization, and functional analysis of the murine estrogen receptor beta (1997) Mol. Endocrinol., 11, pp. 353-365
Foidart, A., Lakaye, B., Grisar, T., Estrogen receptor-beta in quail: Cloning, tissue expression and neuroanatomical distribution (1999) J. Neurobiol., 40, pp. 327-342
Ball, G.F., Bernard, D.J., Foidart, A., Steroid sensitive sites in the avian brain: Does the distribution of the estrogen receptor alpha and beta types provide insight into their function? (1999) Brain Behav. Evol., 54, pp. 28-40
Kim, Y.S., Stumpf, W.E., Sar, M., Martinez-Vargas, M.C., Estrogen and androgen target cells in the brain of fishes, reptiles, and birds: Phylogeny and ontogeny (1978) Am. Zool., 18, pp. 425-433
Martinez-Vargas, M.C., Stumpf, W.E., Sar, M., Estrogen localization in the dove brain. Phylogenetic considerations and implications for nomenclature (1975) Anatomical Neuroendocrinology, pp. 166-175. , W.E. Stumpf & P.P. Grant, Eds.: Karger. Basel
Martinez-Vargas, M.C., Stumpf, W.E., Sar, M., Anatomical distribution of estrogen target cells in the avian CNS: A comparison with the mammalian CNS (1976) J. Comp. Neurol., 167, pp. 83-104
Watson, J.T., Adkins-Regan, E., Neuroanatomical localization of sex steroid-concentrating cells in the Japanese quail (Coturnix japonica): Autoradiography with [3H]- testosterone, [3H]-estradiol, and [3H]-dihydrotestosterone (1989) Neuroendocrinology, 49, pp. 51-64
Brenowitz, E.A., Arnold, A.P., Accumulation of estrogen in a vocal control brain region of a duetting song bird (1989) Brain Res., 480, pp. 119-125
Nordeen, K.W., Nordeen, E.J., Arnold, A.P., Estrogen accumulation in zebra finch song control nuclei: Implications for sexual differentiation and adult activation of song behavior (1987) J. Neurobiol., 18, pp. 569-582
Gahr, M., Flügge, G., Güttinger, H.R., Immunocytochemical localization of estrogen binding neurons in the songbird brain (1987) Brain Res., 402, pp. 173-177
Jacobs, E.C., Arnold, A.P., Campagnoni, A.T., Zebra finch estrogen receptor cDNA: Cloning and mRNA expression (1996) J. Steroid Biochem. Mol. Biol., 59, pp. 135-145
Kuiper, G.G.J.M., Shughrue, P.J., Merchenthaler, I., Gustaffson, J.-A., The estrogen receptor b subtype: A novel mediator of estrogen action in neuroendocrine systems (1998) Front. Neuroendocrinol., 19, pp. 253-286
Thompson, R.R., Goodson, J.L., Ruscio, M.G., Adkins-Regan, E., Role of the archistriatal nucleus taeniae in the sexual behavior of male Japanese quail (Coturnix japonica): A comparison of function with the medial nucleus of the amygdala in mammals (1998) Brain Behav. Evol., 51, pp. 215-229
Bottjer, S.W., The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches (1993) J. Neurobiol., 24, pp. 51-69
Soha, J.A., Shimizu, T., Doupe, A.J., Development of the catecholaminergic innervation of the song system of the male zebra finch (1996) J. Neurobiol., 29, pp. 473-489
Mello, C.V., Pinaud, R., Ribeiro, S., Noradrenergic system of the zebra finch brain: Immunocytochemical study of dopamine-beta-hydroxylase (1998) J. Comp. Neurol., 400, pp. 207-228
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 (2001) Cell Tissue Res., 304, pp. 237-259
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 (1988) Brain Res., 459, pp. 333-343
Barclay, S.R., Harding, C.F., Differential modulation of monoamine levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches (1990) Brain Res., 523, pp. 251-262
Sakaguchi, H., Saito, N., The acetylcholine and catecholamine contents in song control nuclei of zebra finch during song ontogeny (1989) Dev. Brain Res., 47, pp. 313-317
Riters, L.V., Ball, G.F., Sex differences in the densities of alpha2-adrenergic receptors in the song control system, but not the medial preoptic nucleus in zebra finches (2002) J. Chem. Neuroanat., 23, pp. 269-277
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 (1994) Psychoneuroendocrinology, 19, pp. 485-504
Riters, L.V., Eens, M., Pinxten, R., Ball, G.F., Seasonal changes in the densities of alpha2-noradrenergic receptors are inversely related to changes in testosterone and the volumes of song control nuclei in male European starlings (2002) J. Comp. Neurol., 444, pp. 63-74
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 (1994) J.Neurobiol., 25, pp. 767-780
Dahlström, A., Fuxe, K., Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurones (1964) Acta Physiol. Scand., 62, pp. 1-55
Reiner, A., Karle, E.J., Anderson, K.D., Medina, L., Catecholaminergic perikarya and fibers in the avian nervous system (1994) Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates, pp. 135-181. , W.J.A.J. Smeets & A. Reiner, Eds.: Cambridge University Press. Cambridge, UK
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 (2000) J. Chem. Neuroanat., 18, pp. 117-133
Appeltants, D., Ball, G.F., Balthazart, J., The origin of catecholaminergic inputs to the song control nucleus RA in canaries (2002) Neuroreport, 13, pp. 649-653
Lewis, J.W., Ryan, S.M., Arnold, A.P., Butcher, L.L., Evidence for catecholamine projection to area X in the zebra finch (1981) J. Comp. Neurol., 196, pp. 347-354
Appeltants, D., Ball, G.F., Balthazart, J., Song activation by testosterone is associated with increased catecholaminergic innervation of the song control system in female canaries (2003) Neuroscience, 121, pp. 801-814
Nottebohm, F., Testosterone triggers growth of brain vocal control nuclei in adult female canaries (1980) Brain Res., 189, pp. 429-436
Grant, L.D., Stumpf, W.E., Hormone uptake sites in CNS biogenic amines systems (1975) Anatomical Neuroendocrinology, pp. 445-463. , W.E. Stumpf, L.D. Grant, Eds.: Karger. Basel
Sar, M., Estradiol is concentrated in tyrosine hydroxylase-containing neurons of the hypothalamus (1984) Science, 223, pp. 938-940
Batailler, M., Blache, D., Thibault, J., Tillet, Y., Immunohistochemical colocalization of tyrosine hydroxylase and estradiol receptors in the sheep arcuate nucleus (1992) Neurosci. Lett., 146, pp. 125-130
Kritzer, M.F., Selective colocalization of immunoreactivity for intracellular gonadal steroid hormone receptors and tyrosine hydroxylase in the ventral tegmental area, substantia nigra, and retrorubral fields in the rat (1997) J. Comp. Neurol., 379, pp. 247-260
Heritage, A.S., Stumpf, W.E., Sar, M., Grant, L.D., Brainstem catecholaminergic neurons are target sites for sex steroid hormones (1980) Science, 207, pp. 1377-1379
Balthazart, J., Ball, G.F., Effects of the noradrenergic neurotoxin DSP-4 on luteinizing hormone levels, catecholamine concentrations, alpha2-adrenergic receptor binding, and aromatase activity in the brain of the Japanese quail (1989) Brain Res., 492, pp. 163-175
Barclay, S.R., Harding, C.F., Waterman, S.A., Correlations between catecholamine levels and sexual behavior in male zebra finches (1991) Pharmacol. Biochem. Behav., 41, pp. 195-201
Barclay, S.R., Harding, C.F., Waterman, S.A., Central DSP-4 treatment decreases norepinephrine levels and courtship behavior in male zebra finches (1996) Pharmacol. Biochem. Behav., 53, pp. 213-220
Blaustein, J.D., Ulster, D.H., Gonadal steroid hormone receptors and social behaviors (1989) Advances in Comparative and Environmental Physiology, 33, pp. 31-104. , J. Balthazart, Ed.: Springer Verlag. Berlin
Blaustein, J.D., Tetel, M.J., Meredith, J.M., Neurobiological regulation of hormonal response by progestin and estrogen receptors (1995) Neurobiological Effects of Sex Steroid Hormones, pp. 324-349. , P.E. Micevych, R.P.J. Hammer, Eds.: Cambridge University Press. Cambridge, UK
Curran, T., Morgan, J.I., Fos: An immediate-early transcription factor in neurons (1995) J. Neurobiol., 26, pp. 403-412
Ball, G.F., Gentner, T.Q., They're playing our song: Gene expression and birdsong perception (1998) Neuron, 21, pp. 271-274
Mello, C.V., Mapping vocal communication pathways in birds with inducible gene expression (2002) J. Comp. Physiol. A, 188, pp. 943-959
Maney, D.L., Ball, G.F., Territorial behavior induces fos-like immunoreactivity in catecholaminergic brain nuclei in free-living song sparrows (2003) J. Neurobiol., 56, pp. 163-170
Appeltants, D., Del Negro, C., Balthazart, J., Noradrenergic control of auditory information processing in female canaries (2002) Behav. Brain Res., 133, pp. 221-235
Jarvis, E.D., Scharff, C., Grossman, M.R., For whom the bird sings: Context-dependent gene expression (1998) Neuron, 21, pp. 775-788
Hessler, N.A., Doupe, A.J., Social context modulates singing-related neural activity in the songbird forebrain (1999) Nat. Neurosci., 2, pp. 209-211
Hessler, N.A., Doupe, A.J., Singing-related neural activity in a dorsal forebrain-basal ganglia circuit of adult zebra finches (1999) J. Neurosci., 19, pp. 10461-10481
Castelino, C.B., Ball, G.F., (2002) Noradrenergic Regulation of Context-dependent Zenk Expression Related to Song Production in Male Zebra Finches, , Society for Neuroscience. Washington, DC. Abstr. 680.9
Brenowitz, E.A., Birdsong: Integrating physics, physiology, and behavior (2002) J. Comp. Physiol., 188, pp. 827-828
Margoliash, D., Evaluating theories of bird song learning: Implications for future directions (2002) J. Comp. Physiol., 188, pp. 851-866
Baxter, M.G., Effects of selective immunotoxic lesions on learning and memory (2001) Methods Mol. Biol., 166, pp. 249-265