ORBi: Detailled Reference

Article (Scientific journals)

Does the syrinx, a peripheral structure, constrain effects of sex steroids on behavioral sex reversal in adult canaries?

Dos Santos, Ednei B; Logue, David M; Ball, Gregory F et al.

2023 • In Hormones and Behavior, 154, p. 105394

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/311545

DOI
10.1016/j.yhbeh.2023.105394

PubMed
37343444

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Dos Santos2023-Syrinx.pdf

Author postprint (3.79 MB)

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Behavioral constraints; Sex differences; Sexual differentiation; Testosterone; Vocal behavior; Gonadal Steroid Hormones; Animals; Female; Male; Gonadal Steroid Hormones/pharmacology; Testosterone/pharmacology; Brain; Sex Characteristics; Canaries/physiology; Vocalization, Animal/physiology; Canaries; Vocalization, Animal; Endocrinology; Endocrine and Autonomic Systems; Behavioral Neuroscience

Abstract :

[en] We previously confirmed that effects of testosterone (T) on singing activity and on the volume of brain song control nuclei are sexually differentiated in adult canaries: females are limited in their ability to respond to T as males do. Here we expand on these results by focusing on sex differences in the production and performance of trills, i.e., rapid repetitions of song elements. We analyzed >42,000 trills recorded over a period of 6 weeks from 3 groups of castrated males and 3 groups of photoregressed females that received Silastic™ implants filled with T, T plus estradiol or left empty as control. Effects of T on the number of trills, trill duration and percent of time spent trilling were all stronger in males than females. Irrespective of endocrine treatment, trill performance assessed by vocal deviations from the trill rate versus trill bandwidth trade-off was also higher in males than in females. Finally, inter-individual differences in syrinx mass were positively correlated with specific features of trills in males but not in females. Given that T increases syrinx mass and syrinx fiber diameter in males but not in females, these data indicate that sex differences in trilling behavior are related to sex differences in syrinx mass and syrinx muscle fiber diameter that cannot be fully suppressed by sex steroids in adulthood. Sexual differentiation of behavior thus reflects organization not only of the brain but also of peripheral structures.

Research Center/Unit :

GIGA Neurosciences-Neuroendocrinology - ULiège

Disciplines :

Neurosciences & behavior

Author, co-author :

Dos Santos, Ednei B ; GIGA Neurosciences, Laboratory of Behavioral Neuroendocrinology, University of Liege, Belgium

Logue, David M ; Department of Psychology, University of Lethbridge, Lethbridge, AB, Canada

Ball, Gregory F ; Department of Psychology, University of Maryland, College Park, MD, USA

Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques

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

Language :

English

Title :

Does the syrinx, a peripheral structure, constrain effects of sex steroids on behavioral sex reversal in adult canaries?

Publication date :

August 2023

Journal title :

Hormones and Behavior

ISSN :

0018-506X

eISSN :

1095-6867

Publisher :

Academic Press Inc., United States

Volume :

154

Pages :

105394

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://api.elsevier.com/content/article/PII:S0018506X23000922?httpAccept=text/xml

Funders :

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., J.B., and C.A.C.). We thank Pr. Robert Dooling and Ed. Smith, Department of Psychology, University of Maryland in College Park for providing the MATLAB script used to analyze canary song. C.A.C. is F.R.S.-FNRS Research Director.

Available on ORBi :

since 19 January 2024

Statistics

Number of views

32 (1 by ULiège)

Number of downloads

0 (0 by ULiège)

More statistics

Scopus citations^®

3

Scopus citations^®
without self-citations

0

OpenCitations

1

OpenAlex citations

5

Bibliography

Adam, I., Elemans, C.P.H., Vocal motor performance in birdsong requires brain-body interaction. eNeuro, 6, 2019.
Alvarez-Borda, B., Nottebohm, F., Gonads and singing play separate, additive roles in new neuron recruitment in adult canary brain. J. Neurosci. 22 (2002), 8684–8690.
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.
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.
Andersson, M., Sexual Selection. 1994, Princeton University Press, Princeton NJ.
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.
Ball, G.F., Balthazart, J., The neuroendocrinology and neurochemistry of birdsong. Lajtha, A., (eds.) Handbook of Neurochemistry and Molecular Neurobiology, 3rd edition, 2007, Springer, New York, 419–457 (J.D. Blaustein, Volume Ed.).
Beach, F.A, The Biopsychology of Development. 1971, Academic Press, New York, 249–296.
Beach, F.A., Historical origins of modern research on hormones and behavior. Horm. Behav. 15 (1981), 325–376.
Brainard, M.S., Doupe, A.J., Auditory feedback in learning and maintenance of vocal behaviour. Nat. Rev. Neurosci. 1 (2000), 31–40.
Cade, B.S., Noon, B.R., A gentle introduction to quantile regression for ecologists. Front. Ecol. Environ. 1 (2003), 412–420.
Catchpole, C.K., Slater, P.J.B., Bird Song. Biological Themes and Variations. 2018, Cambridge University Press, Cambridge, UK.
Christensen, L.A., Allred, L.M., Goller, F., Meyers, R.A., Is sexual dimorphism in singing behavior related to syringeal muscle composition?. Auk 134 (2017), 710–720.
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.
Cornez, G., Collignon, C., Muller, W., Cornil, C.A., Ball, G.F., Balthazart, J., Development of perineuronal nets during ontogeny correlates with sensorimotor vocal learning in canaries. eNeuro, 7, 2020.
Dos Santos, E.B., Ball, G.F., Cornil, C.A., Balthazart, J., Treatment with androgens plus estrogens cannot reverse sex differences in song and the song control nuclei in adult canaries. Horm. Behav., 143, 2022, 105197.
Draganoiu, T.I., Nagle, L., Kreutzer, M., Directional female preference for an exaggerated male trait in canary (Serinus canaria) song. Proc. Biol. Sci. 269 (2002), 2525–2531.
Elemans, C.P., Mead, A.F., Rome, L.C., Goller, F., Superfast vocal muscles control song production in songbirds. PLoS One, 3, 2008, e2581.
Fuxjager, M.J., Eaton, J., Lindsay, W.R., Salwiczek, L.H., Rensel, M.A., Barske, J., Sorenson, L., Day, L.B., Schlinger, B.A., Evolutionary patterns of adaptive acrobatics and physical performance predict expression profiles of androgen receptor – but not oestrogen receptor – in the forelimb musculature. Funct. Ecol. 29 (2015), 1197–1208.
Gadagkar, V., Puzerey, P.A., Chen, R., Baird-Daniel, E., Farhang, A.R., Goldberg, J.H., Dopamine neurons encode performance error in singing birds. Science 354 (2016), 1278–1282.
Geraci, M., Linear quantile mixed models: the lqmm package for Laplace quantile regression. J. Stat. Softw. 57 (2014), 1–29.
Goldman, S.A., Nottebohm, F., Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. U. S. A. 80 (1983), 2390–2394.
Goller, F., Vocal atheletics — from birdsong production mechanisms to sexy songs. Anim. Behav. 184 (2022), 173–184.
Griffiths, R., Double, M.C., Orr, K., Dawson, R.J., A DNA test to sex most birds. Mol. Ecol. 7 (1998), 1071–1075.
Haakenson, C.M., Madison, F.N., Ball, G.F., Effects of song experience and song quality on immediate early gene expression in female canaries (Serinus canaria). Dev. Neurobiol. 79 (2019), 521–535.
Hartog, T.E., Dittrich, F., Pieneman, A.W., Jansen, R.F., Frankl-Vilches, C., Lessmann, V., Lilliehook, C., Goldman, S.A., Gahr, M., Brain-derived neurotrophic factor signaling in the HVC is required for testosterone-induced song of female canaries. J. Neurosci. 29 (2009), 15511–15519.
Howe, M.W., Tierney, P.L., Sandberg, S.G., Phillips, P.E., Graybiel, A.M., Prolonged dopamine signalling in striatum signals proximity and value of distant rewards. Nature 500 (2013), 575–579.
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.
Kirkpatrick, M., Ryan, M.J., The evolution of mating preferences and the paradox of the lek. Nature 350 (1991), 33–38.
Leboucher, G., Kreutzer, M., Dittami, J., Copulation-solicitation displays in female canaries (Serinus canaria): are oestradiol implants necessary?. Ethology 97 (1994), 190–197.
Leitner, S., Voigt, C., Metzdorf, R., Catchpole, C.K., Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J. Neurobiol. 64 (2005), 275–284.
Li, X.C., Jarvis, E.D., Alvarez-Borda, B., Lim, D.A., Nottebohm, F., A relationship between behavior, neurotrophin expression, and new neuron survival. PNAS 97 (2000), 8584–8589.
Logue, D.M., Sheppard, J.A., Walton, B., Brinkman, B.E., Medina, O.J., An analysis of avian vocal performance at the note and song levels. Bioacoustics 29 (2020), 709–730.
Louissaint, A.J., Rao, S., Leventhal, C., Goldman, S.A., Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron 34 (2002), 945–960.
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.
Maxwell, A., Adam, I., Larsen, P.S., Sorensen, P.G., Elemans, C.P.H., Syringeal vocal folds do not have a voice in zebra finch vocal development. Sci. Rep., 11, 2021, 6469.
Monbureau, M., Barker, J.M., Leboucher, G., Balthazart, J., Male song quality modulates c-Fos expression in the auditory forebrain of the female canary. Physiol. Behav. 147 (2015), 7–15.
Nottebohm, F., Arnold, A.P., Sexual dimorphism in vocal control areas of the songbird brain. Science 194 (1976), 211–213.
Owren, M.J., Berkowitz, M., Bachorowski, J.A., Listeners judge talker sex more efficiently from male than from female vowels. Percept. Psychophys. 69 (2007), 930–941.
Phoenix, C.H., Goy, R.W., Gerall, A.A., Young, W.C., Organizational action of prenatally administered testosterone propionate on the tissues mediating behavior in the female guinea pig. Endocrinology 65 (1959), 369–382.
Podos, J., A performance constraint on the evolution of trilled vocalizations in a songbird family (Passeriformes: Emberizidae). Evolution 51 (1997), 537–551.
Podos, J., Correlated evolution of morphology and vocal signal structure in Darwin's finches. Nature 409 (2001), 185–188.
Podos, J., Sung, H.-C., Vocal performance in songbirds: from mechanisms to evolution. Sakata, J.T., Woolley, S.C., Fay, R.R., Popper, A.N., (eds.) The Neuroethology of Birdsong, Springer Handbook of Auditory Research, 2020, 245–268.
Podos, J., Lahti, D.C., Moseley, D.L., Vocal performance and sensorimotor learning in songbirds. Advances in the Study of Animal Behavior, 2009, Academic Press, 159–195.
Prince, B., Riede, T., Goller, F., Sexual dimorphism and bilateral asymmetry of syrinx and vocal tract in the European starling (Sturnus vulgaris). J. Morphol. 272 (2011), 1527–1536.
R Team, RStudio: Integrated Development for R. 2021.
Rehsteiner, U., Geisser, H., Reyer, H., Singing and mating success in water pipits: one specific song element makes all the difference. Anim. Behav. 55 (1998), 1471–1481.
Sakata, J.T., Vehrencamp, S.L., Integrating perspectives on vocal performance and consistency. J. Exp. Biol. 215 (2012), 201–209.
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.
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.Y., White, D.J., Hartenstein, V., Eliceiri, K., Tomancak, P., Cardona, A., Fiji: an open-source platform for biological-image analysis. Nat. Methods 9 (2012), 676–682.
Schlinger, B.A., Brenowitz, E.A., Neural and hormonal control of birdsong. Pfaff, D.W., Joels, M., (eds.) Hormones, Brain and Behavior, 3rd ed., 2017, Academic Press, Oxford, 255–290.
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.
Suthers, R.A., Vallet, E., Kreutzer, M., Bilateral coordination and the motor basis of female preference for sexual signals in canary song. J. Exp. Biol. 215 (2012), 2950–2959.
Tobet, S.A., Fox, T.O., Sex differences in neuronal morphology influenced hormonally throughout life. Gerall, A.A., Moltz, H., Ward, I.L., (eds.) Handbook of Behavioral Neurobiology. Vol 11. Sexual Differentiation, 0 ed., 1992, Plenum Press, New York, 41–83.
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.
Umemoto, S., Yanagihara, S., Okanoya, K., Durations of preparatory motor activity in the avian basal ganglia for songs and calls in a species of songbirds. Neurosci. Res. 181 (2022), 66–73.
Vallet, E., Kreutzer, M., Female canaries are sexually responsive to special song phrases. Anim. Behav. 49 (1995), 1603–1610.
Vallet, E., Beme, I.I., Kreutzer, M., Two-note syllables in canary songs elicit high levels of sexual display. Anim. Behav. 55 (1998), 291–297.
Veney, S.L., Wade, J., Steroid receptors in the adult zebra finch syrinx: a sex difference in androgen receptor mRNA, minimal expression of estrogen receptor alpha and aromatase. Gen. Comp. Endocrinol. 136 (2004), 192–199.
Veney, S.L., Wade, J., Post-hatching syrinx development in the zebra finch: an analysis of androgen receptor, aromatase, estrogen receptor alpha and estrogen receptor beta mRNAs. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191 (2005), 97–104.
Wade, J., Buhlman, L., Lateralization and effects of adult androgen in a sexually dimorphic neuromuscular system controlling song in zebra finches. J. Comp. Neurol. 426 (2000), 154–164.
Wickham, H., Chang, W., ggplot2: an implementation of the grammar of graphics. https://ggplot2-book.org/introduction.html, 2008.
Wilson, D.R., Bitton, P.-P., Podos, J., Uneven sampling and the analysis of vocal performance constraints. Am. Nat. 183 (1997), 214–228.
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.

Similar publications