[en] Steroid hormones regulate multiple but distinct aspects of social behaviors. Testosterone (T) has multiple effects on learned courtship song in that it regulates both the motivation to sing in a particular social context as well as the quality of song produced. The neural substrate(s) where T acts to regulate the motivation to sing as opposed to other aspects of song has not been definitively characterized. We show here that T implants in the medial preoptic nucleus (POM) of castrated male canaries (Serinus canaria) increase song rate but do not enhance acoustic features such as song stereotypy compared with birds receiving peripheral T that can act globally throughout the brain. Strikingly, T action in the POM increased song control nuclei volume, consistent with the hypothesis that singing activity induces neuroplasticity in the song control system independent of T acting in these nuclei. When presented with a female canary, POM-T birds copulated at a rate comparable to birds receiving systemic T but produced fewer calls and songs in her presence. Thus, POM is a key site where T acts to activate copulation and increase song rate, an appetitive sexual behavior in songbirds, but T action in other areas of the brain or periphery (e.g., HVC, dopaminergic cell groups, or the syrinx) is required to enhance the quality of song (i.e., stereotypy) as well as regulate context-specific vocalizations. These results have broad implications for research concerning how steroids act at multiple brain loci to regulate distinct sociosexual behaviors and the associated neuroplasticity.
Disciplines :
Zoology Neurosciences & behavior
Author, co-author :
Alward, Beau A.
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Ball, Gregory F.
Language :
English
Title :
Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate.
Publication date :
2013
Journal title :
Proceedings of the National Academy of Sciences of the United States of America
ISSN :
0027-8424
eISSN :
1091-6490
Publisher :
National Academy of Sciences, Washington, United States - District of Columbia
Adkins-Regan E (2009) Neuroendocrinology of social behavior. ILAR J 50(1): 5-14.
Ball GF, Riters LV, Balthazart J (2002) Neuroendocrinology of song behavior and avian brain plasticity: Multiple sites of action of sex steroid hormones. Front Neuroendocrinol 23(2): 137-178.
Bottjer SW, Johnson F (1997) Circuits, hormones, and learning: Vocal behavior in songbirds. J Neurobiol 33(5): 602-618.
Lee AW, Pfaff DW (2008) Hormone effects on specific and global brain functions. J Physiol Sci 58(4): 213-220.
Arnold AP (1981) Logical levels of steroid hormone action in the control of vertebrate behavior. American Zoologist 21: 233-242.
Alexander GM, Sherwin BB (1991) The association between testosterone, sexual arousal, and selective attention for erotic stimuli in men. Horm Behav 25(3): 367-381.
Ball GF, Hulse SH (1998) Birdsong. Am Psychol 53(1): 37-58.
Nottebohm F, Stokes TM, Leonard CM (1976) Central control of song in the canary, Serinus canarius. J Comp Neurol 165(4): 457-486.
Vicario DS, Simpson HB (1995) Electrical stimulation in forebrain nuclei elicits learned vocal patterns in songbirds. J Neurophysiol 73(6): 2602-2607.
Vu ET, Mazurek ME, Kuo YC (1994) Identification of a forebrain motor programming network for the learned song of zebra finches. J Neurosci 14(11 Pt 2): 6924-6934.
Thompson CK, Bentley GE, Brenowitz EA (2007) Rapid seasonal-like regression of the adult avian song control system. Proc Natl Acad Sci USA 104(39): 15520-15525.
Nottebohm F (1981) A brain for all seasons: Cyclical anatomical changes in song control nuclei of the canary brain. Science 214(4527): 1368-1370.
Tramontin AD, Brenowitz EA (2000) Seasonal plasticity in the adult brain. Trends Neurosci 23(6): 251-258.
Alvarez-Borda B, Nottebohm F (2002) Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain. J Neurosci 22(19): 8684-8690.
Sartor JJ, Ball GF (2005) Social suppression of song is associated with a reduction in volume of a song-control nucleus in European starlings (Sturnus vulgaris). Behav Neurosci 119(1): 233-244.
Larson TA, et al. (2013) Postsynaptic neural activity regulates neuronal addition in the adult avian song control system. Proc Natl Acad Sci USA 110(41): 16640-16644.
Nottebohm F (2002) Why are some neurons replaced in adult brain? J Neurosci 22(3): 624-628.
Ball GF, et al. (2004) Seasonal plasticity in the song control system: Multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann N Y Acad Sci 1016: 586-610.
Boseret G, Carere C, Ball GF, Balthazart J (2006) Social context affects testosteroneinduced singing and the volume of song control nuclei in male canaries (Serinus canaria). J Neurobiol 66(10): 1044-1060.
Tramontin AD, Wingfield JC, Brenowitz EA (1999) Contributions of social cues and photoperiod to seasonal plasticity in the adult avian song control system. J Neurosci 19(1): 476-483.
Bernard DJ, Wilson FE, Ball GF (1997) Testis-dependent and -independent effects of photoperiod on volumes of song control nuclei in American tree sparrows (Spizella arborea). Brain Res 760(1-2): 163-169.
Gulledge CC, Deviche P (1998) Photoperiod and testosterone independently affect vocal control region volumes in adolescent male songbirds. J Neurobiol 36(4): 550-558.
Fee MS, Scharff C (2010) The songbird as a model for the generation and learning of complex sequential behaviors. ILAR J 51(4): 362-377.
Bernard DJ, Bentley GE, Balthazart J, Turek FW, Ball GF (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(10): 4633-4643.
DeVoogd TJ (1986) Steroid interactions with structure and function of avian song control regions. J Neurobiol 17(3): 177-201.
Pintér O, Péczely P, Zsebok S, Zelena D (2011) Seasonal changes in courtship behavior, plasma androgen levels and in hypothalamic aromatase immunoreactivity in male free-living European starlings (Sturnus vulgaris). Gen Comp Endocrinol 172(1): 151-157.
Thompson CK (2011) Cell death and the song control system: A model for how sex steroid hormones regulate naturally-occurring neurodegeneration. Dev Growth Differ 53(2): 213-224.
Meitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ (2007) Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 27(44): 12045-12057.
Brenowitz EA, 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(19): 12421-12426.
Balthazart J, Surlemont C (1990) Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol Behav 48(5): 599-609.
Davidson JM (1966) Activation of the male rat's sexual behavior by intracerebral implantation of androgen. Endocrinology 79(4): 783-794.
Paredes RG (2003) Medial preoptic area/anterior hypothalamus and sexual motivation. Scand J Psychol 44(3): 203-212.
Watson JT, Adkins-Regan E (1989) Testosterone implanted in the preoptic area of male Japanese quail must be aromatized to activate copulation. Horm Behav 23(3): 432-447.
Riters LV, Ball GF (1999) Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Horm Behav 36(3): 276-286.
Harding CF (2004) Hormonal modulation of singing: Hormonal modulation of the songbird brain and singing behavior. Ann N Y Acad Sci 1016: 524-539.
Maney DL, Pinaud R (2011) Estradiol-dependent modulation of auditory processing and selectivity in songbirds. Front Neuroendocrinol 32(3): 287-302.
McCall C, Singer T (2012) The animal and human neuroendocrinology of social cognition, motivation and behavior. Nat Neurosci 15(5): 681-688.
Schlinger BA (1997) Sex steroids and their actions on the birdsong system. J Neurobiol 33(5): 619-631.
Lieberburg I, Nottebohm F (1979) High-affinity androgen binding proteins in syringeal tissues of songbirds. Gen Comp Endocrinol 37(3): 286-293.
Arnold AP, Nottebohm F, Pfaff DW (1976) Hormone concentrating cells in vocal control and other areas of the brain of the zebra finch (Poephila guttata). J Comp Neurol 165(4): 487-511.
Gahr M (2001) Distribution of sex steroid hormone receptors in the avian brain: Functional implications for neural sex differences and sexual behaviors. Microsc Res Tech 55(1): 1-11.
Riters LV, Absil P, Balthazart J (1998) Effects of brain testosterone implants on appetitive and consummatory components of male sexual behavior in Japanese quail. Brain Res Bull 47(1): 69-79.
Wood RI, Newman SW (1995) The medial amygdaloid nucleus and medial preoptic area mediate steroidal control of sexual behavior in the male Syrian hamster. Horm Behav 29(3): 338-353.
Kingsbury MA, Kelly AM, Schrock SE, Goodson JL (2011) Mammal-like organization of the avian midbrain central gray and a reappraisal of the intercollicular nucleus. PLoS One 6(6):e20720.
Newman SW (1999) The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann N Y Acad Sci 877: 242-257.
Adkins-Regan E (2005) Activity dependent brain plasticity: Does singing increase the volume of a song system nucleus? Theoretical comment on Sartor and Ball (2005). Behav Neurosci 119(1): 346-348.
Charlier TD, Ball GF, Balthazart J (2008) Rapid action on neuroplasticity precedes behavioral activation by testosterone. Horm Behav 54(4): 488-495.
Riters LV, et al. (2000) Seasonal changes in courtship song and the medial preoptic area in male European starlings (Sturnus vulgaris). Horm Behav 38(4): 250-261.
Appeltants D, Absil P, Balthazart J, Ball GF (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(3): 117-133.
Appeltants D, Ball GF, Balthazart J (2002) The origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport 13(5): 649-653.
Riters LV, Alger SJ (2004) Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: Possible neural substrates for sexually motivated song. Cell Tissue Res 316(1): 35-44.
Li XC, Jarvis ED, Alvarez-Borda B, Lim DA, Nottebohm F (2000) A relationship between behavior, neurotrophin expression, and new neuron survival. Proc Natl Acad Sci USA 97(15): 8584-8589.
Beach FA (1948) Hormones and Behavior (Paul B. Hoeber, New York).
Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J Biol Rhythms 16(4): 365-380.
Derégnaucourt S, Mitra PP, Fehér O, Pytte C, Tchernichovski O (2005) How sleep affects the developmental learning of bird song. Nature 433(7027): 710-716.
Tchernichovski O, Nottebohm F, Ho CE, Pesaran B, Mitra PP (2000) A procedure for an automated measurement of song similarity. Anim Behav 59(6): 1167-1176.
Alward BA, Rouse ML, Stevenson TJ, Ball GF (2012) Photoperiodic and social regulation of song rate and structure in male border canaries (Serinus canaria). Integrative and Comparative Biology 52:E5 (abstr).
Voigt C, Leitner S (2008) Seasonality in song behaviour revisited: Seasonal and annual variants and invariants in the song of the domesticated canary (Serinus canaria). Horm Behav 54(3): 373-378.
Marler PR, Slabbekoorn H (2004) Nature's Music: The Science of Birdsong (Academic, San Diego).
Stokes TM, Leonard CM, Nottebohm F (1974) The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J Comp Neurol 156(3): 337-374.
Sartor JJ, Balthazart J, Ball GF (2005) Coordinated and dissociated effects of testosterone on singing behavior and song control nuclei in canaries (Serinus canaria). Horm Behav 47(4): 467-476.
Nottebohm F, Arnold AP (1976) Sexual dimorphism in vocal control areas of the songbird brain. Science 194(4261): 211-213.
McCasland JS (1987) Neuronal control of bird song production. J Neurosci 7(1): 23-39.
Bernard DJ, Eens M, Ball GF (1996) Age- and behavior-related variation in volumes of song control nuclei in male European starlings. J Neurobiol 30(3): 329-339.