Rapid testosterone-induced growth of the medial preoptic nucleus in male canaries.

[en] Testosterone activates singing within days in castrated male songbirds but full song quality only develops after a few weeks. Lesions of the medial preoptic nucleus (POM) inhibit while stereotaxic testosterone implants into this nucleus increase singing rate suggesting that this site plays a key role in the regulation of singing motivation. Testosterone action in the song control system works in parallel to control song quality. Accordingly, systemic testosterone increases POM volume within 1-2days in female canaries, while the increase in volume of song control nuclei takes at least 2weeks. The current study tested whether testosterone action is associated with similar differences in latencies in males. Photosensitive castrated male canaries were implanted with testosterone-filled Silastic implants and control castrates received empty implants, while simultaneously the photoperiod was switched from short- to long-days. Brains were collected from all subjects two days later. Plasma testosterone was elevated in testosterone-treated but not in controls. HVC volumes were not affected, but testosterone significantly increased the POM volume as identified by the dense group of aromatase-immunoreactive neurons, the number and somal area of these neurons and the fractional area they cover in POM. Testosterone-treated females from a previous experiment had a smaller POM volume in similar conditions suggesting the existence of a stable sex difference potentially affecting singing behavior. Thus testosterone induces male POM growth and aromatase expression in this nucleus within two days without affecting HVC size, further supporting the notion that testosterone increases singing motivation via its action in POM.

Research Center/Unit :

Giga-Neurosciences - ULiège

Disciplines :

Neurosciences & behavior

Author, co-author :

Shevchouk, Olesya T.

Ball, Gregory F.

Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau

Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques

Language :

English

Title :

Rapid testosterone-induced growth of the medial preoptic nucleus in male canaries.

Publication date :

2019

Journal title :

Physiology and Behavior

ISSN :

0031-9384

eISSN :

1873-507X

Publisher :

Elsevier, New-York, United States - New York

Volume :

204

Pages :

20-26

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

PAI

Commentary :

Available on ORBi :

since 23 April 2019

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Bibliography

Catchpole, C.K., Slater, P.J.B., Bird Song: Biological Themes and Variations. 2008, Cambridge University Press, Cambridge, UK.
Collins, S., Vocal fighting and flirting: the functions of birdsong. Marler, P., Slabbekoorn, H., (eds.) Nature's Lusic, the Science of Birdsong, 2004, Elsevier, Amsterdam, 39–79.
Schlinger, B.A., Sex steroids and their actions on the birdsong system. J. Neurobiol. 33 (1997), 619–631.
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.
Ball, G.F., Balthazart, J., Neuroendocrine regulation of reproductive behavior in birds. Hormones, Brain and Behavior Online, 2010, 855–897.
Schlinger, B.A., Brenowitz, E.A., Neural and hormonal control of birdsong. Pfaff, D.W., Joels, M., (eds.) Hormones, Brain and Behavior, 3, 2017, Academic Press, Oxford, 255–290.
Nottebohm, F., Testosterone triggers growth of brain vocal control nuclei in adult female canaries. Brain Res. 189 (1980), 429–436.
Sartor, J.J., Balthazart, J., Ball, G.F., Coordinated and dissociated effects of testosterone on singing behavior and song control nuclei in canaries (Serinus canaria). Horm. Behav. 47 (2005), 467–476.
Madison, F.N., Rouse, M.L. Jr., Balthazart, J., Ball, G.F., Reversing song behavior phenotype: testosterone driven induction of singing and measures of song quality in adult male and female canaries (Serinus canaria). Gen. Comp. Endocrinol. 215 (2015), 61–75.
Harding, C.F., Hormonal modulation of singing: hormonal modulation of the songbird brain and singing behavior. Ann. N. Y. Acad. Sci. 1016 (2004), 524–539.
Zeigler, H.P., Marler, P., Neuroscience of Birdsong. 2008, Cambridge University Press, Cambridge, UK.
Yamamura, T., Barker, J.M., Balthazart, J., Ball, G.F., Androgens and estrogens synergistically regulate the expression of doublecortin and enhance neuronal recruitment in the song system of adult female canaries. J. Neurosci. 31 (2011), 9649–9657.
Brenowitz, E.A., Plasticity of the song control system in adult birds. Zeigler, H.P., Marler, P., (eds.) Neuroscience of Birdsong, 2008, Cambridge University Press, Cambridge, 332–349.
Brenowitz, E.A., Larson, T.A., Neurogenesis in the adult avian song-control system. Cold Spring Harb. Perspect. Biol., 7, 2015, a019000.
Balthazart, J., Ball, G.F., Endocrine and social regulation of adult neurogenesis in songbirds. Front. Neuroendocrinol. 41 (2016), 3–22.
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. 27 (2007), 12045–12057.
Alward, B.A., Balthazart, J., Ball, G.F., Dissociable effects on birdsong of androgen signaling in cortex-like brain regions of Canaries. J. Neurosci. 37 (2017), 8612–8624.
Panzica, G.C., Viglietti-Panzica, C., Balthazart, J., The sexually dimorphic medial preoptic nucleus of quail: a key brain area mediating steroid action on male sexual behavior. Front. Neuroendocrinol. 17 (1996), 51–125.
Balthazart, J., Ball, G.F., Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front. Neuroendocrinol. 28 (2007), 161–178.
Alward, B.A., Balthazart, J., Ball, G.F., Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 19573–19578.
Riters, L.V., Ball, G.F., Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Horm. Behav. 36 (1999), 276–286.
Alger, S.J., Riters, L.V., 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 (2006), 1326–1336.
Alward, B.A., Madison, F.N., Parker, S.E., Balthazart, J., Ball, G.F., Pleiotropic control by testosterone of a learned vocal behavior and its underlying neuroplasticity(1,2,3). eNeuro., 3, 2016.
Charlier, T.D., Ball, G.F., Balthazart, J., Rapid action on neuroplasticity precedes behavioral activation by testosterone. Horm. Behav. 54 (2008), 488–495.
Shevchouk, O.T., Ghorbanpoor, S., Ball, G.F., Cornil, C.A., Balthazart, J., Testosterone-induced neuroendocrine changes in the medial preoptic area precede song activation and plasticity in song control nuclei of female canaries. Eur. J. Neurosci. 45 (2017), 886–900.
Shevchouk, O.T., Ghorbanpoor, S., Smith, E., Liere, P., Schumacher, M., Ball, G.F., et al. Behavioral evidence for sex steroids hypersensitivity in castrated male canaries. Horm. Behav. 103 (2018), 80–96.
Shevchouk, O.T., Ball, G.F., Cornil, C.A., Balthazart, J., Studies of HVC plasticity in adult canaries reveal social effects and sex differences as well as limitations of multiple markers available to assess adult Neurogenesis. PLoS One, 12, 2017, e0170938.
Luine, V., Nottebohm, F., Harding, C.F., McEwen, B.S., Androgen affects cholinergic enzymes in syringeal motor neurons and muscles. Brain Res. 192 (1980), 89–107.
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. 20 (2000), 854–861.
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. 57 (2003), 130–140.
Hall, Z.J., MacDougall-Shackleton, E.A., Influence of testosterone metabolites on song-control system neuroplasticity during photostimulation in adult European starlings (Sturnus vulgaris). PLoS One, 7, 2012, e40060.
Appeltants, D., Ball, G.F., Balthazart, J., Song activation by testosterone is associated with an increased catecholaminergic innervation of the song control system in female canaries. Neuroscience 121 (2003), 801–814.
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.
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. J. Neurobiol. 54 (2003), 370–379.
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. 104 (2007), 15520–15525.
Smith, G.T., Brenowitz, E.A., Wingfield, J.C., Seasonal changes in the size of the avian song control nucleus HVC defined by multiple histological markers. J. Comp. Neurol. 381 (1997), 253–261.
Balthazart, J., Surlemont, C., Harada, N., Aromatase as a cellular marker of testosterone action in the preoptic area. Physiol. Behav. 51 (1992), 395–409.
Foidart, A., de Clerck, A., Harada, N., Balthazart, J., Aromatase-immunoreactive cells in the quail brain: effects of testosterone and sex dimorphism. Physiol. Behav. 55 (1994), 453–464.
Alward, B.A., Rouse, M.L., Balthazart, J., Ball, G.F., Testosterone regulates birdsong in an anatomically specific manner. Anim. Behav. 124 (2017), 291–298.
Harding, C.F., Sheridan, K., Walters, M.J., Hormonal specificity and activation of sexual behavior in male zebra finches. Horm. Behav. 17 (1983), 111–133.
Harding, C.F., Walters, M.J., Collado, D., Sheridan, K., Hormonal specificity and activation of social behavior in male red-winged blackbirds. Horm. Behav. 22 (1988), 402–418.
Fusani, L., Gahr, M., Hormonal influence on song structure and organization: the role of estrogen. Neuroscience 138 (2006), 939–946.
Alward, B.A., de Bournonville, C., Chan, T.T., Balthazart, J., Cornil, C.A., Ball, G.F., Aromatase inhibition rapidly affects in a reversible manner distinct features of birdsong. Sci. Rep., 6, 2016, 32344.
Panzica, G.C., Viglietti-Panzica, C., Calagni, M., Anselmetti, G.C., Schumacher, M., Balthazart, J., Sexual differentiation and hormonal control of the sexually dimorphic medial preoptic nucleus in the quail. Brain Res. 416 (1987), 59–68.