Testosterone-induced neuroendocrine changes in the medial preoptic area precede song activation and plasticity in song control nuclei of female canaries
Shevchouk, Olesya; Ghorbanpoor, Samar; Ball, Gregory Fet al.
2017 • In European Journal of Neuroscience, 45 (7), p. 886-900
[en] Testosterone plays a key role in the control of seasonal changes in singing behavior and its underlying neural circuitry. After administration of exogenous testosterone, song quality and song control nuclei volumes change over the course of weeks, but song rate increases within days. The medial preoptic nucleus (POM) controls sexual motivation and testosterone action in POM increases sexually motivated singing. Here, we investigated the time course of testosterone action in the song control nuclei and POM, at the gross anatomical and cellular level. Photosensitive female canaries were injected with BrdU to label newborn neurons. One day later they were transferred to a long day photoperiod and implanted with testosterone-filled or empty implants. Brains and blood were collected 1, 2, 9 or 21 days later. Testosterone increased POM volume within one day, whereas the volume of song control nuclei increased significantly only on day 21 even if a trend was already observed for HVC on day 9. The density of newborn neurons in HVC, labeled by Bromodeoxyuridine (BrdU) and doublecortin, was increased by testosterone on days 9 and 21 although a trend was already detectable on day 2. In POM testosterone increased the number and size of aromatase-immunoreactive neurons already after one day. This rapid action of testosterone in POM supports its proposed role in controlling singing motivation. Although testosterone increased the number of newborn neurons in HVC rapidly (9, possibly 2 days), it is unlikely that these new neurons affect singing behavior before they mature and integrate into functional circuits.
Research center :
Giga-Neurosciences - ULiège
Disciplines :
Neurosciences & behavior
Author, co-author :
Shevchouk, Olesya ; Université de Liège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Ghorbanpoor, Samar
Ball, Gregory F
Cornil, Charlotte ; Université de Liège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Balthazart, Jacques ; Université de Liège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Language :
English
Title :
Testosterone-induced neuroendocrine changes in the medial preoptic area precede song activation and plasticity in song control nuclei of female canaries
Publication date :
2017
Journal title :
European Journal of Neuroscience
ISSN :
0953-816X
eISSN :
1460-9568
Publisher :
Blackwell Science, Paris, France
Volume :
45
Issue :
7
Pages :
886-900
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
BELSPO - SPP Politique scientifique - Service Public Fédéral de Programmation Politique scientifique
Alger, S.J. & Riters, L.V. (2006) Lesions to the medial preoptic nucleus differentially affect singing and nest box-directed behaviors within and outside of the breeding season in European starlings (Sturnus vulgaris). Behav. Neurosci., 120, 1326–1336.
Alvarez-Borda, B. & Nottebohm, F. (2002) Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain. J. Neurosci., 22, 8684–8690.
Alvarez-Buylla, A. & Kirn, J.R. (1997) Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J. Neurobiol., 33, 585–601.
Alvarez-Buylla, A. & Nottebohm, F. (1988) Migration of young neurons in adult avian brain. Nature, 335, 353–354.
Alvarez-Buylla, A., Theelen, M. & Nottebohm, F. (1990) Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron, 5, 101–109.
Alward, B.A., Balthazart, J. & Ball, G.F. (2013) Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate. Proc. Natl. Acad. Sci. USA, 110, 19573–19578.
Alward, B.A., Balthazart, J. & Ball, G.F. (2016a) Pleiotropic actions of steroid hormones in the regulation of birdsong. Abstract SBN Montreal 2016. P1.19.
Alward, B.A., de Bournonville, C., Chan, T.T., Balthazart, J., Cornil, C.A. & Ball, G.F. (2016b) Aromatase inhibition rapidly affects in a reversible manner distinct features of birdsong. Sci. Rep., 6, 32344.
Alward, B.A., Madison, F.N., Parker, S.E., Balthazart, J. & Gregory, F. (2016c) Pleiotropic control by testosterone of a learned vocal behavior and its underlying neuroplasticity. eNeuro, 3, 1–17.
Alward, B.A., Rouse, M.L., Balthazart, J. & Ball, G.F. (2016d) Testosterone regulates birdsong in an anatomically specific manner. Anim. Behav., doi:10.1016/j.anbehav.2016.09.013 [Epub ahead of print].
Appeltants, D., Absil, P., Balthazart, J. & Ball, G.F. (2000) Identification of the origin of catecholaminergic inputs to HVc in canaries by retrograde tract tracing combined with tyrosine hydroxylase immunocytochemistry. J. Chem. Neuroanat., 18, 117–133.
Appeltants, D., Ball, G.F. & Balthazart, J. (2002) The origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport, 13, 649–653.
Appeltants, D., Ball, G.F. & Balthazart, J. (2003) Song activation by testosterone is associated with an increased catecholaminergic innervation of the song control system in female canaries. Neuroscience, 121, 801–814.
Aste, N., Viglietti-Panzica, C., Balthazart, J. & Panzica, G.C. (1997) Testosterone modulation of peptidergic pathways in the septo-preoptic region of male Japanese quail. Poult. Avian Biol. Rev., 8, 77–93.
Bahr, J.M., Wang, S.C., Huang, M.Y. & Calvo, F.O. (1983) Steroid concentrations in isolated theca and granulosa layers of preovulatory follicles during the ovulatory cycle of the domestic hen. Biol. Reprod., 29, 326–334.
Ball, G.F. & Balthazart, J. (2010) Seasonal and hormonal modulation of neurotransmitter systems in the song control circuit. J. Chem. Neuroanat., 39, 82–95.
Balthazart, J. & Ball, G.F. (2007) Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front. Neuroendocrin., 28, 161–178.
Balthazart, J. & Ball, G.F. (2016) Endocrine and social regulation of adult neurogenesis in songbirds. Front. Neuroendocrin., 41, 3–22.
Balthazart, J. & Foidart, A. (1993) Brain aromatase and the control of male sexual behavior. J. Steroid Biochem., 44, 521–540.
Balthazart, J., Foidart, A. & Hendrick, J.C. (1990) The induction by testosterone of aromatase activity in the preoptic area and activation of copulatory behavior. Physiol. Behav., 47, 83–94.
Balthazart, J., Surlemont, C. & Harada, N. (1992) Aromatase as a cellular marker of testosterone action in the preoptic area. Physiol. Behav., 51, 395–409.
Balthazart, J., Absil, P., Foidart, A., Houbart, M., Harada, N. & Ball, G.F. (1996a) Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J. Neurobiol., 31, 129–148.
Balthazart, J., Tlemçani, O. & Harada, N. (1996b) Localization of testosterone-sensitive and sexually dimorphic aromatase-immunoreactive cells in the quail preoptic area. J. Chem. Neuroanat., 11, 147–171.
Balthazart, J., Absil, P., Gérard, M., Appeltants, D. & Ball, G.F. (1998) Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J. Neurosci., 18, 6512–6527.
Balthazart, J., Boseret, G., Konkle, A.T.M., Hurley, L.L. & Ball, G.F. (2008) Doublecortin as a marker of adult neuroplasticity in the canary song control nucleus HVC. Eur. J. Neurosci., 27, 801–817.
Barami, K., Kirschenbaum, B., Lemmon, V. & Goldman, S.A. (1994) N-Cadherin and Ng-CAM/8D9 are involved serially in the migration of newly generated neurons into the adult songbird brain. Neuron, 13, 567–582.
Barami, K., Iversen, K., Furneaux, H. & Goldman, S.A. (1995) Hu protein as an early marker of neuronal phenotypic differentiation by subependymal zone cells of the adult songbird forebrain. J. Neurobiol., 28, 82–101.
Barker, J.M., Ball, G.F. & Balthazart, J. (2014) Anatomically discrete sex differences and enhancement by testosterone of cell proliferation in the telencephalic ventricle zone of the adult canary brain. J. Chem. Neuroanat., 22, 1–8.
Barker, J.M., Charlier, T.D., Ball, G.F. & Balthazart, J. (2013) A new method for in vitro detection of bromodeoxyuridine in serum: a proof of concept in a songbird species, the canary. PLoS One, 8, 1–5.
Bernard, D.J., Wilson, F.E. & Ball, G.F. (1997) Testis-dependent and -independent effects of photoperiod on volumes of song control nuclei in American tree-sparrows (Spizella arborea). Brain Res., 760, 163–169.
Bernard, D.J., Bentley, G.E., Balthazart, J., Turek, F.W. & Ball, G.F. (1999) Androgen receptor, estrogen receptor alpha, and estrogen receptor beta show distinct patterns of expression in forebrain song control nuclei of European starlings. Endocrinology, 140, 4633–4643.
Boseret, G., Carere, C., Ball, G.F. & Balthazart, J. (2006) Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria). J. Neurobiol., 66, 1044–1060.
Brenowitz, E.A. & Larson, T.A. (2015) Neurogenesis in the adult avian. Cold Spring Harb. Perspect. Biol., 7, 1–23.
Brenowitz, E.A. & Lent, K. (2001) Afferent input is necessary for seasonal growth and maintenance of adult avian song control circuits. J. Neurosci., 21, 2320–2329.
Brenowitz, E.A. & Lent, K. (2002) Act locally and think globally: intracerebral testosterone implants induce seasonal-like growth of adult avian song control circuits. Proc. Natl. Acad. Sci. USA, 99, 12421–12426.
Brown, S.D., Johnson, F. & Bottjer, S.W. (1993) Neurogenesis in adult canary telencephalon is independent of gonadal hormone levels. J. Neurosci., 13, 2024–2032.
Catchpole, C.K. & Slater, P.J.B. (2008) Bird Song. Biological Themes and Variations. Cambridge University Press, Cambridge, UK.
Charlier, T.D., Ball, G.F. & Balthazart, J. (2008) Rapid action on neuroplasticity precedes behavioral activation by testosterone. Horm. Behav., 54, 488–495.
Charlier, T.D., Harada, N., Balthazart, J. & Cornil, C.A. (2011) Human and quail aromatase activity is rapidly and reversibly inhibited by phosphorylating conditions. Endocrinology, 152, 4199–4210.
Collins, S. (2004). Vocal fighting and flirting: the functions of birdsong. In Marler, P. & Slabbekoorn, H. (Eds), Nature's Music, The Science of Birdsong. Elsevier, Amsterdam, pp. 39–79.
Cornez, G., Ter Haar, S.M., Cornil, C.A. & Balthazart, J. (2015) Anatomically discrete sex differences in neuroplasticity in zebra finches as reflected by perineuronal nets. PLoS One, 10, 1–19.
Desjardins, C. & Turek, F.W. (1977) Effects of testosterone on spermatogenesis and luteinizing hormone release in Japanese quail. Gen. Comp. Endocr., 33, 293–303.
DeVoogd, T.J. & Nottebohm, F. (1981) Gonadal hormones induce dendritic growth in the adult brain. Science, 214, 202–204.
DeVries, M.S., Cordes, M.A., Stevenson, S.A. & Riters, L.V. (2015) Differential relationships between D1 and D2 dopamine receptor expression in the medial preoptic nucleus and sexually-motivated song in male European starlings (Sturnus vulgaris). Neuroscience, 301, 289–297.
Foidart, A., De Clerck, A., Harada, N. & Balthazart, J. (1994) Aromatase-immunoreactive cells in the quail brain: effects of testosterone and sex dimorphism. Physiol. Behav., 55, 453–464.
Foidart, A., Reid, J., Absil, P., Yoshimura, N., Harada, N. & Balthazart, J. (1995) Critical re-examination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. J. Chem. Neuroanat., 8, 267–282.
Francis, F., Koulakoff, A., Boucher, D., Chafey, P., Schaar, B., Vinet, M.C., Friocourt, G., McDonnell, N. et al. (1999) Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron, 23, 247–256.
Fusani, L. (2008) Endocrinology in field studies: problems and solutions for the experimental design. Gen. Comp. Endocr., 157, 249–253.
Fusani, L. & Gahr, M. (2006) Hormonal influence on song structure and organization: the role of estrogen. Neuroscience, 138, 939–946.
Fusani, L., Hutchison, J.B. & Gahr, M. (2001) Testosterone regulates the activity and expression of aromatase in the canary neostriaturn. J. Neurobiol., 49, 1–8.
Fusani, L., Metzdorf, R., Hutchison, J.B. & Gahr, M. (2003) Aromatase inhibition affects testosterone-induced masculinization of song and the neural song system in female canaries. J. Neurobiol., 54, 370–379.
Goldman, S.A. & Nottebohm, F. (1983) Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. USA, 80, 2390–2394.
Goodson, J.L. (1998) Territorial aggression and dawn song are modulated by septal vasotocin and vasoactive intestinal polypeptide in male field sparrows (Spizella pusilla). Horm. Behav., 34, 67–77.
Goodson, J.L., Eibach, R., Sakata, J. & Adkins-Regan, E. (1999) Effect of septal lesions on male song and aggression in the colonial zebra finch (Taeniopygia guttata) and the territorial field sparrow (Spizella pusilla). Behav. Brain Res., 98, 167–180.
Guigueno, M.F., Sherry, D.F. & MacDougall-Shackleton, S.A. (2016) Sex and seasonal differences in neurogenesis and volume of the song-control system are associated with song in brood-parasitic and non-brood-parasitic icterid songbirds. Dev. Neurobiol., 76, 1226–1240.
Hall, Z.J. & MacDougall-Shackleton, S.A. (2012) Influence of testosterone metabolites on song-control system neuroplasticity during photostimulation in adult european starlings (Sturnus vulgaris). PLoS One, 7, e40060.
Harding, C.F. (2004) Hormonal modulation of singing: hormonal modulation of the songbird brain and singing behavior. Ann. NY Acad. Sci., 1016, 305–319.
Harding, C.F., Sheridan, K. & Walters, M.J. (1983) Hormonal specificity and activation of sexual behavior in male zebra finches. Horm. Behav., 17, 111–133.
Harding, C.F., Walters, M.J., Collado, D. & Sheridan, K. (1988) Hormonal specificity and activation of social behavior in male red-winged blackbirds. Horm. Behav., 22, 402–418.
Hartog, T.E., Dittrich, F., Pieneman, A.W., Jansen, R.F., Frankl-Vilches, C., Lessmann, V., Lilliehook, C., Goldman, S.A. et al. (2009) Brain-derived neurotrophic factor signaling in the HVC is required for testosterone-induced song of female canaries. J. Neurosci., 29, 15511–15519.
Hayes, N.L. & Nowakowski, R.S. (2002) Dynamics of cell proliferation in the adult dentate gyrus of two inbred strains of mice. Brain Res. Dev. Brain Res., 134, 77–85.
Heimovics, S.A., Cornil, C.A., Ball, G.F. & Riters, L.V. (2009) D1-like dopamine receptor density in nuclei involved in social behavior correlates with song in a context-dependent fashion in male European starlings. Neuroscience, 159, 962–973.
Hidalgo, A., Barami, K., Iversen, K. & Goldman, S.A. (1995) 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., 27, 470–487.
Hurley, L.L., Wallace, A.M., Sartor, J.J. & Ball, G.F. (2008) Photoperiodic induced changes in reproductive state of border canaries (Serinus canaria) are associated with marked variation in hypothalamic gonadotropin-releasing hormone immunoreactivity and the volume of song control regions. Gen. Comp. Endocr., 158, 10–19.
Jiang, J., McMurtry, J., Niedzwiecki, D. & Goldman, S.A. (1998) Insulin-like growth factor-1 is a radial cell-associated neurotrophin that promotes neuronal recruitment from the adult songbird ependyma/subependyma. J. Neurobiol., 36, 1–15.
Johnson, A.L. (1986) Reproduction in the female. In Sturkie, P.D. (Ed.), Avian Physiology, 4th Edn. Springer-Verlag, New York, Berlin, Heidelberg, Tokyo, pp. 403–431.
Kelm-Nelson, C.A. & Riters, L.V. (2013) Curvilinear relationships between mu-opioid receptor labeling and undirected song in male European starlings (Sturnus vulgaris). Brain Res., 1527, 29–39.
Kirn, J.R., Fishman, Y., Sasportas, K., Alvarez-Buylla, A. & Nottebohm, F. (1999) Fate of new neurons in adult canary high vocal center during the first 30 days after their formation. J. Comp. Neurol., 411, 487–494.
Ko, M.-C., Frankl-Vilches, C., Bakker, A. & Gahr, M. (2015) The last hours before singing: Short-term dynamic transcriptomes after testosterone treatment in female canaries. Abstract Soc Neurosci Chicago 2015, nbr. 344.03/Y7.
Louissaint, A.J., Rao, S., Leventhal, C. & Goldman, S.A. (2002) Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron, 34, 945–960.
Luine, V., Nottebohm, F., Harding, C.F. & McEwen, B.S. (1980) Androgen affects cholinergic enzymes in syringeal motor neurons and muscles. Brain Res., 192, 89–107.
Lynch, K.S., Diekamp, B. & Ball, G.F. (2008) Catecholaminergic cell groups and vocal communication in male songbirds. Physiol. Behav., 93, 870–876.
Madison, F.N., Rouse, M.L., Balthazart, J. & Ball, G.F. (2015) Reversing song behavior phenotype: testosterone driven induction of singing and measures of song quality in adult male and female canaries (Serinus canaria). Gen. Comp. Endocr., 215, 61–75.
Maney, D.L. & Ball, G.F. (2003) Fos-like immunoreactivity in catecholaminergic brain nuclei after territorial behavior in free-living song sparrows. J. Neurobiol., 56, 163–170.
Maney, D.L., Bernard, D.J. & Ball, G.F. (2001) Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem. Neurosci. Lett., 311, 189–192.
Meitzen, J., Moore, I.T., Lent, K., Brenowitz, E.A. & Perkel, D.J. (2007) Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J. Neurosci., 27, 12045–12057.
Meitzen, J., Thompson, C.K., Choi, H., Perkel, D.J. & Brenowitz, E.A. (2009) Time course of changes in Gambel's white-crowned sparrow song behavior following transitions in breeding condition. Horm. Behav., 55, 217–227.
Monks, D.A., Getsios, S., MacCalman, C.D. & Watson, N.V. (2001a) N-cadherin is regulated by gonadal steroids in the adult hippocampus. Proc. Natl. Acad. Sci. USA, 98, 1312–1316.
Monks, D.A., Getsios, S., MacCalman, C.D. & Watson, N.V. (2001b) N-cadherin is regulated by gonadal steroids in adult sexually dimorphic spinal motoneurons. J. Neurobiol., 47, 255–264.
Mouriec, K. & Balthazart, J. (2013) Peripubertal proliferation of progenitor cells in the preoptic area of Japanese quail (Coturnix japonica). Brain Res., 1516, 20–32.
Norstedt, G., Levinovitz, A. & Eriksson, H. (1989) Regulation of uterine insulin-like growth factor I mRNA and insulin-like growth factor II mRNA by estrogen in the rat. Acta Endocrinol. (Cop), 120, 466–472.
Nottebohm, F. (1981) A brain for all seasons: cyclical anatomical changes in song-control nuclei of the canary brain. Science, 214, 1368–1370.
Nottebohm, F., Stokes, T.M. & Leonard, C.M. (1976) Central control of song in the canary, Serinus canarius. J. Comp. Neurol., 165, 457–486.
Nottebohm, F., O'Loughlin, B., Gould, K., Yohay, K. & Alvarez-Buylla, A. (1994) 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. USA, 91, 7849–7853.
Panzica, G.C., Viglietti-Panzica, C., Sanchez, F., Sante, P. & Balthazart, J. (1991) Effects of testosterone on a selected neuronal population within the preoptic sexually dimorphic nucleus of the Japanese quail. J. Comp. Neurol., 303, 443–456.
Panzica, G.C., Viglietti-Panzica, C. & Balthazart, J. (1996) The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrin., 17, 51–125.
Quispe, R., Trappschuh, M., Gahr, M. & Goymann, W. (2015) Towards more physiological manipulations of hormones in field studies: comparing the release dynamics of three kinds of testosterone implants: silastic tubing, time-release pellets and beeswax. Gen. Comp. Endocr., 212, 100–105.
Rasika, S., Nottebohm, F. & Alvarez-Buylla, A. (1994) Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc. Natl. Acad. Sci. USA, 91, 7854–7858.
Riters, L.V. & Ball, G.F. (1999) Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Horm. Behav., 36, 276–286.
Riters, L.V., Eens, M., Pinxten, R., Duffy, D.L., Balthazart, J. & Ball, G.F. (2000) Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm. Behav., 38, 250–261.
Roark, E.F., Paradies, N.E., Lagunowich, L.A. & Grunwald, G.B. (1992) Evidence for endogenous proteases, mRNA level and insulin as multiple mechanisms of N-cadherin down-regulation during retinal development. Development, 114, 973–984.
Rouse, M.L. Jr, Stevenson, T.J., Fortune, E.S. & Ball, G.F. (2015) Reproductive state modulates testosterone-induce singing in adult female European starlings (Sturnus vulgaris). Horm. Behav., 72, 78–87.
Sahlin, L., Norstedt, G. & Eriksson, H. (1994) Estrogen regulation of the estrogen receptor and insulinlike growth factor-I in the rat uterus: a potential coupling between effects of estrogen and IGF-I. Steroids, 59, 421–430.
Shevchouk, O.T., Ball, G.F., Cornil, C.A. & Balthazart, J. (2017) Studies of HVC plasticity in adult canaries reveal social effects and sex differences as well as limitations of multipe markers available to assess adult neurogenesis. Plos One, 12, e0170938.
Smith, G.T., Brenowitz, E.A., Beecher, M.D. & Wingfield, J.C. (1997) Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J. Neurosci., 17, 6001–6010.
Steel, E., Follett, B.K. & Hinde, R.A. (1975) The role of short days in the termination of photorefractoriness in female canaries (Serinus canarius). J. Endocrinol., 64, 451–464.
Steimer, T. & Hutchison, J.B. (1981) Androgen increases formation of behaviourally effective oestrogen in dove brain. Nature, 292, 345–347.
Stratton, L.G., Ewing, L.L. & Desjardins, C. (1973) Efficacy of testosterone-filled polydimethylsiloxane implants in maintaining plasma testosterone in rabbits. J. Reprod. Fertil., 35, 235–244.
Thompson, C.K. & Brenowitz, E.A. (2005) Seasonal change in neuron size and spacing but not neuronal recruitment in a basal ganglia nucleus in the avian song control system. J. Comp. Neurol., 481, 276–283.
Thompson, C.K., Bentley, G.E. & Brenowitz, E.A. (2007) Rapid seasonal-like regression of the adult avian song control system. Proc. Natl. Acad. Sci. USA, 104, 15520–15525.
Tramontin, A.D. & Brenowitz, E.A. (1999) A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning. J. Neurobiol., 40, 316–326.
Tramontin, A.D. & Brenowitz, E.A. (2000) Seasonal plasticity in the adult brain. Trends Neurosci., 23, 251–258.
Tramontin, A.D., Hartman, V.N. & Brenowitz, E.A. (2000) Breeding conditions induce rapid and sequential growth in adult avian song control circuits: a model of seasonal plasticity in the brain. J. Neurosci., 20, 854–861.
Tramontin, A.D., Wingfield, J.C. & Brenowitz, E.A. (2003) Androgens and estrogens induce seasonal-like growth of song nuclei in the adult songbird brain. J. Neurobiol., 57, 130–140.
Turek, F.W., Desjardins, C. & Menaker, M. (1976) Antigonadal and progonadal effects of testosterone in male house sparrows. Gen. Comp. Endocr., 28, 395–402.
Vellema, M., van der Linden, A. & Gahr, M. (2010) Area-specific migration and recruitment of new neurons in the adult songbird brain. J. Comp. Neurol., 518, 1442–1459.
Voorhuis, T.A.M., Kiss, J.Z., de Kloet, E.R. & de Wied, D. (1988) Testosterone-sensitive vasotocin-immunoreactive cells and fibers in the canary brain. Brain Res., 442, 139–146.
Walton, C., Pariser, E. & Nottebohm, F. (2012) The zebra finch paradox: song is little changed, but number of neurons doubles. J. Neurosci., 32, 761–774.
Williams, S., Leventhal, C., Lemmon, V., Nedergaard, M. & Goldman, S.A. (1999) Estrogen promotes the initial migration and inception of NgCAM-dependent calcium-signaling by new neurons of the adult songbird brain. Mol. Cell Neurosci., 13, 41–55.
Yamamura, T., Barker, J.M., Balthazart, J. & Ball, G.F. (2011) Androgens and estrogens synergistically regulate the expression of doublecortin and enhance neuronal recruitment in the song system of adult female canaries. J. Neurosci., 31, 9649–9657.