Testosterone; flutamide; lateral magnocellular nucleus of the anterior nidopallium; song variability, Serinus canaria; Androgens; Receptors, Androgen; Flutamide; Androgen Antagonists; Animals; Male; Stereotyped Behavior/drug effects; Stereotyped Behavior/physiology; Receptors, Androgen/metabolism; Receptors, Androgen/physiology; Flutamide/pharmacology; Photoperiod; Seasons; Signal Transduction/physiology; Signal Transduction/drug effects; Testosterone/metabolism; Testosterone/pharmacology; Androgen Antagonists/pharmacology; Vocalization, Animal/physiology; Vocalization, Animal/drug effects; Canaries/physiology; Androgens/pharmacology
Abstract :
[en] During breeding when testosterone concentrations are high, male songbirds that are open-ended vocal learners like canaries (Serinus canaria) tend to produce a stable, stereotyped song that facilitates mate attraction or territory defense. Outside breeding contexts, song becomes more variable. The neuroendocrine mechanisms controlling this vocal variability across seasons are not entirely clear. We tested whether androgen signaling within the lateral magnocellular nucleus of the anterior nidopallium (LMAN), a cortical-like brain region of the vocal control system known as a vocal variability generator, plays a role in seasonal vocal variability. We first characterized song in birds housed alone on a short day (SD) photoperiod, which simulates non-breeding conditions. Then, cannulae filled with the androgen receptor (AR) blocker flutamide or left empty as control were implanted bilaterally in LMAN. Birds were then transferred to long days (LD) to simulate the breeding season and song was analyzed again. Blocking AR in LMAN increased acoustic variability of song and the acoustic variability of syllables. However, blocking AR in LMAN did not impact the variability of syllable usage nor their sequencing in LD birds, song features that are controlled by androgen signaling in a somatosensory brain region of the vocal control system called HVC. These findings highlight the multifactorial, non-redundant actions of steroid hormones in controlling complex social behaviors such as birdsong. They also support the hypothesis that LMAN is a key brain area for the effects of testosterone on song plasticity both seasonally in adults and during the song crystallization process at sexual maturity.
Disciplines :
Zoology Neurology
Author, co-author :
Alward, Beau A; Department of Psychology, T.I.M.E.S, University of Houston, Houston, TX 77204, USA, Department of Biology and Biochemistry, University of Houston, Houston, TX 77004, USA, Department of Psychology, Neural and Cognitive Science Program, University of Maryland, College Park, MD 20742, USA
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Ball, Gregory F; Department of Psychology, Neural and Cognitive Science Program, University of Maryland, College Park, MD 20742, USA
Language :
English
Title :
Androgen signaling in LMAN regulates song stereotypy in male canaries.
NINDS - National Institute of Neurological Disorders and Stroke
Funding text :
This work was supported by a grant from the National Institute of Neurological Disorders and Stroke Grant RO1NS104008 (to G.F.B. and J.B.). We thank Farrah Madison for logistical support on stereotaxic surgeries and song analysis and Tara Tronetti for assistance on song analysis.
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. USA 110 (2013), 19573–19578.
Alward, B.A., Mayes, W.D., Peng, K., Stevenson, T.J., Balthazart, J., Ball, G.F., Dissociable effects of social context on song and doublecortin immunoreactivity in male canaries. Eur. J. Neurosci. 40 (2014), 2941–2947.
Alward, B.A., Madison, F.N., Gravley, W.T., Ball, G.F., Antagonism of syringeal androgen receptors reduces the quality of female-preferred male song in canaries. Anim. Behav. 119 (2016), 201–212.
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.
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.
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.
Arnold, A.P., Nottebohm, F., Pfaff, D.W., Hormone concentrating cells in vocal control areas of the brain of the zebra finch (Poephila guttata). J. Comp. Neurol. 165 (1976), 487–512.
Aronov, D., Andalman, A.S., Fee, M.S., A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science 320 (2008), 630–634.
Ball, G.F., Chemical neuroanatomical studies of the steroid-sensitive songbird vocal control system: a comparative approach. Balthazart, J., (eds.) Hormones, Brain and Behaviour in Vertebrates. 1. Sexual Differentiation, Neuroanatomical Aspects, Neurotransmitters and Neuropeptides. Comp. Physiol, vol 8, 1990, Karger, Basel, 148–167.
Ball, G.F., Balthazart, J., The neuroendocrinology and neurochemistry of birdsong. Lajtha, A., (eds.) Handbook of Neurochemistry and Molecualr Neurobiology, 3rd Edition, J.D. Blaustein (Volume Ed.), 2007, Springer, New York, 419–457.
Ball, G.F., Madison, F.N., Balthazart, J., Alward, B.A., How does testosterone act to regulate a multifaceted adaptive response? Lessons from studies of the avian song system. J. Neuroendocrinol., 32, 2020, e12793.
Balthazart, J., Surlemont, C., Androgen and estrogen action in the preoptic area and activation of copulatory behavior in quail. Physiol. Behav. 48 (1990), 599–609.
Balthazart, J., Surlemont, C., Copulatory behavior is controlled by the sexually dimorphic nucleus of the quail POA. Brain Res. Bull. 25 (1990), 7–14.
Balthazart, J., Foidart, A., Wilson, E.M., Ball, G.F., Immunocytochemical localization of androgen receptors in the male songbird and quail brain. J.Comp.Neurol. 317 (1992), 407–420.
Bernard, D.J., Bentley, G.E., Balthazart, J., Turek, F.W., Ball, G.F., Androgen receptor, estrogen receptor α, and estrogen receptor β show distinct patterns of expression in forebrain song control nuclei of european starlings. Endocrinology 140 (1999), 4633–4643.
Boseret, G., Carere, C., Ball, G.F., Balthazart, J., Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria). J. Neurobiol. 66 (2006), 1044–1060.
Bottjer, S.W., Hewer, S.J., Castration and antisteroid treatment impair vocal learning in male zebra finches. J. Neurobiol. 23 (1992), 337–353.
Bottjer, S.W., Johnson, F., Circuits, hormones, and learning: Vocal behavior in songbirds. J.Neurobiol. 33 (1997), 602–618.
Bottjer, S.W., Miesner, E.A., Arnold, A.P., Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224 (1984), 901–903.
Brainard, M.S., The anterior forebrain pathway and vocal plasticity. Ziegler, H.P., Marler, P., (eds.) Neuroscience of birdsong, 2008, Cambridge University Press, Cambridge MA, 240–255.
Brenowitz, E.A., Evolution of the vocal control system in the avian brain. Semin. Neurosci. 3 (1991), 399–407.
Brenowitz, E.A., Baptista, L.F., Lent, K., Wingfield, J.C., Seasonal plasticity of the song control system in wild Nuttall's white-crowned sparrows. J.Neurobiol. 34 (1998), 69–82.
Catchpole, C.K., Slater, P.J.B., Bird song. 2008, Cambridge University Press, Cambridge UK, Biological themes and Variations.
Cornez, G., Collignon, C., Müller, W., Ball, G.F., Cornil, C.A., Balthazart, J., Seasonal changes of perineuronal nets and song learning in adult canaries (Serinus canaria). Behav. Brain Res., 380, 2020, 112437.
Cornez, G., Shevchouk, O.T., Ghorbanpoor, S., Ball, G.F., Cornil, C.A., Balthazart, J., Testosterone stimulates perineuronal nets development around parvalbumin cells in the adult canary brain in parallel with song crystallization. Horm. Behav., 119, 2020, 104643.
Dos Santos, E.B., Logue, D.M., Ball, G.F.C.C.A., Balthazart, J., Does the syrinx, a peripheral structure, constrain effects of sex steroids on behavioral sex reversal in adult canaries?. Horm. Behav., 154, 2023, 105394.
Fee, M.S., Goldberg, J.H., A hypothesis for basal ganglia-dependent reinforcement learning in the songbird. Neuroscience 198 (2011), 152–170.
Fee, M.S., Scharff, C., The songbird as a model for the generation and learning of complex sequential behaviors. ILAR J. 51 (2010), 362–377.
Fuxjager, M.J., Schultz, J.D., Barske, J., Feng, N.Y., Fusani, L., Mirzatoni, A., Day, L.B., Hau, M., Schlinger, B.A., Spinal motor and sensory neurons are androgen targets in an acrobatic bird. Endocrinology 153 (2012), 3780–3791.
Gahr, M., Metzdorf, R., Distribution and dynamics in the expression of androgen and estrogen receptors in vocal control systems of songbirds. Brain Res.Bull. 44 (1997), 509–517.
Gahr, M., Güttinger, H.-R., Kroodsma, D.E., Estrogen receptors in the avian brain: Survey reveals general distribution and forebrain areas unique to songbirds. J.Comp.Neurol. 327 (1993), 112–122.
Grisham, W., Park, S.H., Hsia, J.K., Kim, C., Leung, M.C., Kim, L., Arnold, A.P., Effects of long-term flutamide treatment during development in zebra finches. Neurosci. Lett. 418 (2007), 92–96.
Hampton, C.M., Sakata, J.T., Brainard, M.S., An avian basal ganglia-forebrain circuit contributes differentially to syllable versus sequence variability of adult Bengalese finch song. J. Neurophysiol. 101 (2009), 3235–3245.
Hurley, L.L., Wallace, A.M., Sartor, J.J., Ball, G.F., 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. Endocrinol. 158 (2008), 10–19.
Iserbyt, A., Eens, M., Baetens, W., Vermeulen, A., Mûller, W., Within- and between-individual (co)variance partitioning reveals limited pleiotropic effects of testosterone on immune function, sexual signaling, and parental investment. Behav. Ecol. Sociobiol., 71, 2017, 74.
Jarvis, E.D., Brains and birdsong. Marler, P., Slabbekoorn, H., (eds.) Nature's music, 2008, The science of birdsong, Elsevier, Amsterdam, 226–271.
Kao, M.H., Doupe, A.J., Brainard, M.S., Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433 (2005), 638–643.
Ketterson, E.D., Nolan, V. Jr., Wolf, L., Ziegenfus, C., Dufty, A.M. Jr., Ball, G.F., Johnsen, T.S., Testosterone and avian life histories: The effect of experimentally elevated testosterone on corticosterone and body mass in dark-eyed juncos. Horm.Behav. 25 (1991), 489–503.
Kojima, S., Kao, M.H., Doupe, A.J., Brainard, M.S., The Avian Basal Ganglia Are a Source of Rapid Behavioral Variation That Enables Vocal Motor Exploration. J. Neurosci. 38 (2018), 9635–9647.
Korsia, S., Bottjer, S.W., Chronic testosterone treatment impairs vocal learning in male zebra finches during a restricted period of development. J.Neurosci. 11 (1991), 2362–2371.
Leitner, S., Voigt, C., Gahr, M., Seasonal changes in the song pattern of the non-domesticated canary (Serinus canaria), a field study. Behaviour 138 (2001), 885–904.
Marler, P., Peters, S., Ball, G.F., Dufty, A.M., Wingfield, J.C., The role of sex steroids in the acquisition and production of birdsong. Nature 336 (1988), 770–772.
Matheson, L.E., Sun, H., Sakata, J.T., Forebrain circuits underlying the social modulation of vocal communication signals. Dev. Neurobiol. 76 (2016), 47–63.
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.
Moorman, S., Ahn, J.R., Kao, M.H., Plasticity of stereotyped birdsong driven by chronic manipulation of cortical-basal ganglia activity. Curr. Biol., 31(2619–2632), 2021, e2614.
Morrell, J.I., Pfaff, D.W., A neuroendocrine approach to brain function: localization of sex steroid concentrating cells in vertebrate brains. Am. Zool. 18 (1978), 447–460.
Morrell, J.I., Kelley, D.B., Pfaff, D.W., Sex steroid binding in the brain of vertebrates. Knigge, K.M., Scott, D.E., Kobayashi, H., Miura, S., Ishii, S., (eds.) Brain-endocrine interactions II, 0 ed., 1975, Karger, Basel, 230–256.
Nicholls, T.J., Storey, C.R., The effect of duration of the daily photoperiod on recovery of photosensitivity in photorefractory canaries (Serinus canarius). Gen. Comp. Endocrinol. 31 (1977), 72–74.
Nottebohm, F., Brain pathways for vocal learning in birds: A review of the first 10 years. Sprague, J.M., Epstein, A.N., (eds.) Progress in Psychobiology and Physiological Psychology, 0 ed., vol. 9, 1980, Academic Press, New York, 85–214.
Nottebohm, F., Stokes, T.M., Leonard, C.M., Central control of song in the canary, Serinus canarius. J.Comp.Neurol. 165 (1976), 457–486.
Nottebohm, F., Nottebohm, M.E., Crane, L., Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. Behav. Neural Biol. 46 (1986), 445–471.
Olveczky, B.P., Andalman, A.S., Fee, M.S., Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol., 3, 2005, e153.
Parker, A.N., Heterospecific vocal mimicry in Cassin's finch (Carpodacus cassinii): a descriptive analysis. PhD Thesis, 2009, University of California.
Reiner, A.D., Perkel, J., Bruce, L., Butler, A., Csillag, A., Kuenzel, W., Medina, L., Paxinos, G., Shimizu, T., Striedter, G., Wild, M., Ball, G.F., Durand, S., Güntürkün, O., Lee, D.W., Mello, C.V., White, S.A., Hough, G., Kubikova, L., Smulders, T.V., Wada, K., Dugas-Ford, J., Husband, S., Yamamoto, K., Yu, J., C., S., E.D., J., 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473, 377–414.
Rouse, M.L. Jr., Ball, G.F., Lesions targeted to the anterior forebrain disrupt vocal variability associated with testosterone-induced sensorimotor song development in adult female canaries, Serinus canaria. Dev. Neurobiol. 76 (2016), 3–18.
Sakata, J.T., Hampton, C.M., Brainard, M.S., Social modulation of sequence and syllable variability in adult birdsong. J. Neurophysiol. 99 (2008), 1700–1711.
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. J.Neurosci. 11 (1991), 2896–2913.
Schmidt, M.F., Wild, J.M., The respiratory-vocal system of songbirds: Anatomy, physiology, and neural control. Holstege, G., Beers, C.M., Subramanian, H.H., (eds.) Progress in Brain research, 2014, Elsevier, Amsterdam, 297–335.
Smith, G.T., Brenowitz, E.A., Wingfield, J.C., Baptista, L.F., Seasonal changes in song nuclei and song behavior in Gambels white-crowned sparrows. J. Neurobiol. 28 (1995), 114–125.
Smith, G.T., Brenowitz, E.A., Prins, G.S., Use of PG-21 immunocytochemistry to detect androgen receptors in the songbird brain. J.Histochem.Cytochem. 44 (1996), 1075–1080.
Soma, K.K., Sullivan, K., Wingfield, J., Combined aromatase inhibitor and antiandrogen treatment decreases territorial aggression in a wild songbird during the nonbreeding season. Gen. Comp. Endocrinol. 115 (1999), 442–453.
Sperry, T.S., Wacker, D.W., Wingfield, J.C., The role of androgen receptors in regulating territorial aggression in male song sparrows. Horm. Behav. 57 (2010), 86–95.
Tchernichovski, O., Marcus, G., Vocal learning beyond imitation: mechanisms of adaptive vocal development in songbirds and human infants. Curr. Opin. Neurobiol. 28 (2014), 42–47.
Thompson, J.A., Basista, M.J., Wu, W., Bertram, R., Johnson, F., Dual pre-motor contribution to songbird syllable variation. J. Neurosci. 31 (2011), 322–330.
Voigt, C., Leitner, S., Seasonality in song behaviour revisited: seasonal and annual variants and invariants in the song of the domesticated canary (Serinus canaria). Horm. Behav. 54 (2008), 373–378.
Whaling, C.S., Nelson, D.A., Marler, P., Testosterone-induced shortening of the storage phase of song development in birds interferes with vocal learning. Dev. Psychobiol. 28 (1995), 367–376.
Wild, J.M., Birdsong: anatomical foundations and central mechanisms of sensorimotor integration. Ziegler, H.P., Marler, P., (eds.) Neuroscience of Birdsong, 2008, Cambridge University Press, New York NY, 136–151.
Williams, H., Mehta, N., Changes in adult zebra pinch song require a forebrain nucleus that is not necessary for song production. J.Neurobiol. 39 (1999), 14–28.
Williams, H., Connor, D.M., Hill, J.W., Testosterone decreases the potential for song plasticity in adult male zebra finches. Horm. Behav. 44 (2003), 402–412.
Woolley, S.C., Kao, M.H., Variability in action: contributions of a songbird cortical-basal ganglia circuit to vocal motor learning and control. Neuroscience 296 (2015), 39–47.
