[en] Variation in environmental factors such as day length and social context greatly affects reproductive behavior and the brain areas that regulate these behaviors. One such behavior is song in songbirds, which males use to attract a mate during the breeding season. In these species the absence of a potential mate leads to an increase in the number of songs produced, while the presence of a mate greatly diminishes singing. Interestingly, although long days promote song behavior, producing song itself can promote the incorporation of new neurons in brain regions controlling song output. Social context can also affect such neuroplasticity in these song control nuclei. The goal of the present study was to investigate in canaries (Serinus canaria), a songbird species, how photoperiod and social context affect song and the incorporation of new neurons, as measured by the microtubule-associated protein doublecortin (DCX) in HVC, a key vocal production brain region of the song control system. We show that long days increased HVC size and singing activity. In addition, male canaries paired with a female for 2 weeks showed enhanced DCX-immunoreactivity in HVC relative to birds housed alone. Strikingly, however, paired males sang fewer songs that exhibited a reduction in acoustic features such as song complexity and energy, compared with birds housed alone, which sang prolifically. These results show that social presence plays a significant role in the regulation of neural and behavioral plasticity in songbirds and can exert these effects in opposition to what might be expected based on activity-induced neurogenesis.
Disciplines :
Zoology Neurosciences & behavior
Author, co-author :
Alward, Beau A.
Mayes, Wade D.
Peng, Katherine
Stevenson, Tyler J.
Balthazart, Jacques ; Université de Liège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Ball, Gregory F.
Language :
English
Title :
Dissociable effects of social context on song and doublecortin immunoreactivity in male canaries.
Publication date :
2014
Journal title :
European Journal of Neuroscience
ISSN :
0953-816X
eISSN :
1460-9568
Publisher :
Blackwell, Oxford, United Kingdom
Volume :
40
Issue :
6
Pages :
2941-7
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
PAI
Commentary :
(c) 2014 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
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., Ling, C.Y. & Nottebohm, F. (1992) High vocal center growth and its relation to neurogenesis, neuronal replacement and song acquisition in juvenile canaries. J. Neurobiol., 23, 396-406.
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.
Ball, G.F. (1999) Neuroendocrine basis of seasonal changes in vocal behavior among songbirds. In Hauser, M. & Konishi, M. (Eds), The Design of Animal Communication, MIT Press, Cambridge, MA, pp. 213-253.
Ball, G.F., Auger, C.J., Bernard, D.J., Charlier, T.D., Sartor, J.J., Riters, L.V. & Balthazart, J. (2006) Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann. NY Acad. Sci., 1016, 586-610.
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.
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.
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.
Boseret, G., Ball, G.F. & Balthazart, J. (2007) The microtubule-associated protein doublecortin is broadly expressed in the telencephalon of adult canaries. J. Chem. Neuroanat., 33, 140-154.
Bottjer, S.W. & Johnson, F. (1997) Circuits, hormones, and learning: vocal behavior in songbirds. J. Neurobiol., 33, 602-618.
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.
Brenowitz, E.A, Margoliash, D. & Nordeen, K.W. (1997) An introduction to birdsong and the avian song system. J. Neurobiol., 33, 495-500.
Brumm, H. (2004) Male-male vocal interactions and the adjustment of song amplitude in a territorial bird. Anim. Behav., 67, 281-286.
Brumm, H. (2013) The impact of environmental noise on song amplitude in a territorial bird. J. Anim. Ecol., 73, 434-440.
Brumm, H. & Slater, P.J.B. (2006) Animals can vary signal amplitude with receiver distance: evidence from zebra finch song. Anim. Behav., 72, 699-705.
Brumm, H. & Todt, D. (2002) Noise-dependent song amplitude regulation in a territorial songbird. Anim. Behav., 63, 891-897.
Buchanan, K.L., Leitner, S., Spencer, K.A., Goldsmith, A.R. & Catchpole, C.K. (2004) Developmental stress selectively affects the song control nucleus HVC in the zebra finch. P. Roy. Soc. B-Biol. Sci., 271, 2381-2386.
Cacioppo, J.T., Berntson, G.G., Sheridan, J.F. & McClintock, M.K. (2000) Multilevel integrative analyses of human behavior: social neuroscience and the complementing nature of social and biological approaches. Psychol. Bull., 126, 829-843.
Catchpole, C.K. & Slater, P.J. (2003) 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.
Cuthill, I.H.A. (1985) Increase in starling song activity with removal of mate. J. Exp. Biol., 33, 326-335.
Cynx, J. & Gell, C. (2004) Social mediation of vocal amplitude in a songbird, Taeniopygia guttata. Anim. Behav., 67, 451-455.
Dawson, A., King, V.M., Bentley, G.E. & Ball, G.F. (2001) Photoperiodic control of seasonality in birds. J. Biol. Rhythm., 16, 365-380.
Fee, M.S. & Goldberg, J.H. (2011) A hypothesis for basal ganglia-dependent reinforcement learning in the songbird. Neuroscience, 198, 152-170.
Fee, M.S. & Scharff, C. (2010) The songbird as a model for the generation and learning of complex sequential behaviors. ILAR J., 51, 362-377.
Gulledge, C.C. & Deviche, P. (1998) Photoperiod and testosterone independently affect vocal control region volumes in adolescent male songbirds. J. Neurobiol., 36, 550-558.
Hinde, R.A. & Matthews, L.H. (1957) The nest-building behaviour of domesticated canaries. P. Zool. Soc. Lond., 131, 1-48.
Hinde, R.A. & Steel, E. (1976) The effect of male song on an estrogen-dependent behavior pattern in the female canary (Serinus canarius). Horm. Behav., 7, 293-304.
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.
Kirn, J.R. (2010) The relationship of neurogenesis and growth of brain regions to song learning. Brain Lang., 115, 29-44.
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.
Kroodsma, D.E. & Byers, B.E. (1991) The function(s) of bird song. Am. Zool., 31, 318-328.
Larson, T.A., Wang, T., Gale, S.D., Miller, K.E., Thatra, N.M., Caras, M.L., Perkel, D.J. & Brenowitz, E.A. (2013) Postsynaptic neural activity regulates neuronal addition in the adult avian song control system. Proc. Natl. Acad. Sci. USA, 110, 16640-16644.
Lehrman, D.S., Brody, P.N. & Wortis, R.P. (1961) The presence of the mate and of nesting material as stimuli for the development of incubation behavior and for gonadotropin secretion in the ring dove (Streptopelia risoria). Endocrinology, 68, 507-516.
Leitão, A., ten Cate, C. & Riebel, K. (2006) Within-song complexity in a songbird is meaningful to both male and female receivers. Anim. Behav., 71, 1289-1296.
Leitner, S. & Catchpole, C.K. (2004) Syllable repertoire and the size of the song control system in captive canaries (Serinus canaria). J. Neurobiol., 60, 21-27.
Li, X.C., Jarvis, E.D., Alvarez-Borda, B., Lim, D.A. & Nottebohm, F. (2000) A relationship between behavior, neurotrophin expression, and new neuron survival. Proc. Natl. Acad. Sci. USA, 97, 8584-8589.
Newman, A.E.M., MacDougall-Shackleton, S.A., An, Y.S., Kriengwatana, B. & Soma, K.K. (2010) Corticosterone and dehydroepiandrosterone have opposing effects on adult neuroplasticity in the avian song control system. J. Comp. Neurol., 518, 3662-3678.
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. (1984) Birdsong as a model in which to study brain processes related to learning. Condor, 86, 227-236.
Nottebohm, F. (1996) A white canary on Mount Acropolis. J. Comp. Physiol. A., 179, 149-156.
Nottebohm, F. (2002) Why are some neurons replaced in adult brain? J. Neurosci., 22, 624-628.
Orr, L. & Hansell, M. (1975) Effect of removal of mate on the singing behaviour of great tits. Anim. Behav., 29, 635-637.
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.
Sartor, J.J. & Ball, G.F. (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, 233-244.
Sockman, K.W., Sewall, K.B., Ball, G.F. & Hahn, T.P. (2005) Economy of mate attraction in the Cassin's finch. Biol. Letters, 1, 34-37.
Stevenson, T.J. & Ball, G.F. (2010) Photoperiodic differences in a forebrain nucleus involved in vocal plasticity: enkephalin immunoreactivity reveals volumetric variation in song nucleus lMAN but not NIf in male European starlings (Sturnus vulgaris). Dev. Neurobiol., 70, 751-763.
Tchernichovski, O., Nottebohm, F., Ho, C., Pesaran, B. & Mitra, P. (2000) A procedure for an automated measurement of song similarity. Anim. Behav., 59, 1167-1176.
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. (2000) Seasonal plasticity in the adult brain. Trends Neurosci., 23, 251-258.
Tramontin, A.D., Wingfield, J.C. & Brenowitz, E.A. (1999) Contributions of social cues and photoperiod to seasonal plasticity in the adult avian song control system. J. Neurosci., 19, 476-483.
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, 373-378.
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.