Neurogenesis; Singing behavior; Song analysis; Song control system; Songbirds; Testosterone; Endocrinology; Endocrine and Autonomic Systems; Behavioral Neuroscience
Abstract :
[en] Temperate-zone birds display marked seasonal changes in reproductive behaviors and the underlying hormonal and neural mechanisms. These changes were extensively studied in canaries (Serinus canaria) but differ between strains. Fife fancy male canaries change their reproductive physiology in response to variations in day length but it remains unclear whether they become photorefractory (PR) when exposed to long days and what the consequences are for gonadal activity, singing behavior and the associated neural plasticity. Photosensitive (PS) male birds that had become reproductively competent (high song output, large testes) after being maintained on short days (SD, 8 L:16D) for 6 months were divided into two groups: control birds remained on SD (SD-PS group) and experimental birds were switched to long days (16 L:8D) and progressively developed photorefractoriness (LD-PR group). During the following 12 weeks, singing behavior (quantitatively analyzed for 3 × 2 hours every week) and gonadal size (repeatedly measured by CT X-ray scans) remained similar in both groups but there was an increase in plasma testosterone and trill numbers in the LD-PR group. Day length was then decreased back to 8 L:16D for LD-PR birds, which immediately induced a cessation of song, a decrease in plasma testosterone concentration, in the volume of song control nuclei (HVC, RA and Area X), in HVC neurogenesis and in aromatase expression in the medial preoptic area. These data demonstrate that Fife fancy canaries readily respond to changes in photoperiod and display a pattern of photorefractoriness following exposure to long days that is associated with marked changes in brain and behavior.
Disciplines :
Neurosciences & behavior
Author, co-author :
Chiver, Ioana ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Ball, Gregory F; Department of Psychology, University of Maryland, College Park, MD, USA
LALLEMAND, François ; Centre Hospitalier Universitaire de Liège - CHU > > Service médical de radiothérapie
Vandries, Laura ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie de la différenciation sexuelle du cerveau
Plumier, Jérôme P; GIGA Neurosciences, University of Liege, Belgium
Cornil, Charlotte ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Neuroendocrinology
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Language :
English
Title :
Photoperiodic control of singing behavior and reproductive physiology in male Fife fancy 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., 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.
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.
Alvarez-Buylla, A., Mechanism of neurogenesis in adult avian brain. Experientia 46 (1990), 948–955.
Alvarez-Buylla, A., Kirn, J.R., Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J. Neurobiol. 33 (1997), 585–601.
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., 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., 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.
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, 2016, 3.
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.
Baker, M., Bottjer, S.W., Arnold, A.P., Sexual dimorphism and lack of seasonal changes in vocal control regions of the white-crowned sparrow brain. Brain Res., 1984, 295.
Ball, G.F., The neuroendocrine basis of seasonal chnages in vocal behavior among songbirds. Hauser, M.D., Konishi, M., (eds.) The Design of Animal Communication, 1999, MIT Press, Cambridge, Mass, 213–254.
Ball, G.F., Balthazart, J., The neuroendocrinology and neurochemistry of birdsong. Lajtha, A., Blaustein, J.D., (eds.) Handbook of Neurochemistry and Molecualr Neurobiology, 3rd edition, 2007, Springer, New York, 419–457 (Volume Ed.).
Ball, G.F., Balthazart, J., Seasonal and hormonal modulation of neurotransmitter systems in the song control circuit. J. Chem. Neuroanat. 39 (2010), 82–95.
Ball, G.F., Balthazart, J., Neuroendocrine regulation of reproductive behavior in birds. Pfaff, D.W., Joels, M., (eds.) Hormones, Brain and Behavior, 3rd ed., 2017, Academic Press, Oxford, 217–254.
Ball, G.F., Riters, L.V., MacDougall-Shackleton, S.A., Balthazart, J., Sex differences in brain and behavior and the neuroendocrine control of the motivation to sing. Zeigler, H.P., Marler, P., (eds.) Neuroscience of Birdsong, 2008, Cambridge, Cambridge, 320–331.
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., Steroid metabolism and the activation of social behavior. Balthazart, J., (eds.) Molecular and Cellular Basis of Social Behavior in Vertebrates, 1989, Springer-Verlag, Berlin, 105–159.
Balthazart, J., Ball, G.F., Endocrine and social regulation of adult neurogenesis in songbirds. Front. Neuroendocrinol. 41 (2016), 3–22.
Balthazart, J., Absil, P., Foidart, A., Houbart, M., Harada, N., Ball, G.F., Distribution of aromatase-immunoreactive cells in the forebrain of zebra finches (Taeniopygia guttata): implications for the neural action of steroids and nuclear definition in the avian hypothalamus. J. Neurobiol. 31 (1996), 129–148.
Balthazart, J., Boseret, G., Konkle, A.T., Hurley, L.L., Ball, G.F., Doublecortin as a marker of adult neuroplasticity in the canary song control nucleus HVC. Eur. J. Neurosci. 27 (2008), 801–817.
Barker, J.M., Ball, G.F., Balthazart, J., Anatomically discrete sex differences and enhancement by testosterone of cell proliferation in the telencephalic ventricle zone of the adult canary brain. J. Chem. Neuroanat. 55 (2014), 1–8.
Beguin, N., Leboucher, G., Kreutzer, M., Sexual preferences for mate song in female canaries (Serinus canaria). Behaviour 135 (1998), 1185–1196.
Bentley, G.E., Audage, N.C., Hanspal, E.K., Ball, G.F., Hahn, T.P., Photoperiodic response of the hypothalamo-pituitary-gonad axis in male and female canaries, Serinus canaria. J. Exp. Zool. 296A (2003), 143–151.
Boseret, G., Ball, G.F., Balthazart, J., The microtubule-associated protein doublecortin is broadly expressed in the telencephalon of adult canaries. J. Chem. Neuroanat. 33 (2007), 140–154.
Bottjer, S.W., Johnson, F., Circuits, hormones, and learning: vocal behavior in songbirds. J. Neurobiol. 33 (1997), 602–618.
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.
Carere, C., Ball, G.F., Balthazart, J., Sex differences in projections from preoptic area aromatase cells to the periaqueductal gray in Japanese quail. J. Comp. Neurol. 500 (2007), 894–907.
Caro, S.P., Lambrechts, M.M., Balthazart, J., Early seasonal development of brain song control nuclei in male blue tits. Neurosci. Lett. 386 (2005), 139–144.
Caro, S.P., Lambrechts, M.M., Chastel, O., Sharp, P.J., Thomas, D.W., Balthazart, J., Simultaneous pituitary-gonadal recrudescence in two corsican populations of male blue tits with asynchronous breeding dates. Horm. Behav. 50 (2006), 347–360.
Catchpole, C.K., Slater, P.J.B., Bird song. Biological Themes and Variations, 2008, Cambridge University Press, Cambridge UK.
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.
Cornez, G., Valle, S., Dos Santos, E.B., Chiver, I., Muller, W., Ball, G.F., Cornil, C.A., Balthazart, J., Perineuronal nets in HVC and plasticity in male canary song. PLoS One, 16, 2021, e0252560.
Cox, P.R., A statistical investigation into bird-song. British Birds 38 (1944), 3–9.
Dawson, A., Sharp, P.J., Photorefractoriness in birds–photoperiodic and non-photoperiodic control. Gen. Comp. Endocrinol. 153 (2007), 378–384.
Dawson, A., King, V.M., Bentley, G.E., Ball, G.F., Photoperiodic control of seasonality in birds. J. Biol. Rhythm. 16 (2001), 365–380.
Eens, M., Understanding the complex song of the European starling: an integrated ethological approach. Adv. Study Anim. Behav. 26 (1997), 355–434.
Eens, M., Pinxten, R., Verheyen, F.R., Variation in singing activity during the breeding cycle of the European starling Sturnus vulgaris. Belg. J. Zool. 124 (1994), 167–174.
Foidart, A., Reid, J., Absil, P., Yoshimura, N., Harada, N., Balthazart, J., Critical re-examination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. J. Chem. Neuroanat. 8 (1995), 267–282.
Fusani, L., Gahr, M., Hormonal influence on song structure and organization: the role of estrogen. Neuroscience 138 (2006), 939–946.
Fusani, L., Van't Hof, T., Hutchison, J.B., Gahr, M., Seasonal expression of androgen receptors, estrogen receptors, and aromatase in the canary brain in relation to circulating androgens and estrogens. J. Neurobiol. 43 (2000), 254–268.
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.
George, J.M., Bell, Z.W., Condliffe, D., Dohrer, K., Abaurrea, T., Spencer, K., Leitao, A., Gahr, M., Hurd, P.J., Clayton, D.F., Acute social isolation alters neurogenomic state in songbird forebrain. Proc. Natl. Acad. Sci. U. S. A. 117 (2020), 23311–23316.
Goldman, S.A., Adult neurogenesis: from canaries to the clinic. J. Neurobiol. 36 (1998), 267–286.
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.
Hahn, T.P., MacDougall-Shackleton, S.A., Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363 (2008), 267–286.
Goller, F., Vocal atheletics - from birdsong production mechanisms to sexy songs. Anim. Behav. 184 (2022), 173–184.
Hahn, T.P., Boswell, T., Wingfield, J.C., Ball, G.F., Temporal flexibility in avian reproduction. Nolan, V.J., (eds.) Current Ornithology, 1997, Plenum Press, New York, 39–80.
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.
Hidalgo, A., Barami, K., Iversen, K., Goldman, S.A., Estrogens and non-estrogenic ovarian influences combine to promote the recruitment and decrease the turnover of new neurons in the adult female canary brain. J. Neurobiol. 27 (1995), 470–487.
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.
Kirn, J., O'Loughlin, B., Kasparian, S., Nottebohm, F., Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 7844–7848.
Kirn, J.R., Alvarez-Buylla, A., Nottebohm, F., Production and survival of projection neurons in a forebrain vocal center of adult male canaries. J. Neurosci. 11 (1991), 1756–1762.
Lallemand, F., Chiver, I., Barros Dos Santos, E., Ball, G.F., Balthazart, J., Repeated assessment of changes in testes size in canaries by X-ray computer tomography. Gen. Comp. Endocrinol., 310, 2021, 113808.
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.
Leitner, S., Van't Hof, T.J., Gahr, M., Flexible reproduction in wild canaries is independent of photoperiod. Gen. Comp. Endocrinol. 130 (2003), 102–108.
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.
Luttge, W.G., Hall, N.R., Differential effectiveness of T and its metabolites in the induction of sexual behavior in two strains of albino mice. Horm. Behav. 4 (1973), 31–43.
Madison, F.N., Shah, N., Ball, G.F., Intraspecific variation in testosterone-induced neuroplasticity in two canary strains. Horm. Behav., 118, 2020, 104617.
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.
Nicholls, T.J., Golsmith, A.R., Dawson, A., Photorefractoriness in birds and comparison with mammals. Physiol. Rev. 68 (1988), 133–176.
Nottebohm, F., A brain for all seasons: cyclical anatomical changes in song-control nuclei of the canary brain. Science 214 (1981), 1368–1370.
Nottebohm, F., Plasticity in the adult avian central nervous system: possible relation between hormones, learning, and brain repair. Handbook of Physiology-The Nervous System, 1987, 85–108.
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.
Rasika, S., Nottebohm, F., Alvarez-Buylla, A., Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 7854–7858.
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.
Riters, L.V., Eens, M., Pinxten, R., Duffy, D.L., Balthazart, J., Ball, G.F., Seasonal changes in courtship song and the medial preoptic area in male european starlings (Sturnus vulgaris). Horm. Behav. 38 (2000), 250–261.
Robinson, J.E., Follett, B.K., Photoperiodism in Japanese quail: the termination of seasonal breeding by photorefractoriness. Proc. R. Soc. Lond. B Biol. Sci. 215 (1982), 95–116.
Sartor, J.J., Ball, G.F., Activity-dependent regulation of seasonal neuroplasticity in the song system of songbirds. Dawson, A., Sharp, P.J., (eds.) Functional Avian Endocrinology, 2005, Narosa Publishing, New Delhi, India, 351–360.
Schlinger, B., Balthazart, J., Aromatase and behavior: concepts gained from studies of aromatase in the avian brain. Balthazart, J., Ball, G.F., (eds.) Brain Aromatase, Estrogens, and Behavior, 2013, Oxford University Press, Oxford, New York, 169–198.
Schlinger, B.A., Sex steroids and their actions on the birdsong system. J. Neurobiol. 33 (1997), 619–631.
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.
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., Cornil, C.A., Balthazart, J., Behavioral evidence for sex steroids hypersensitivity in castrated male canaries. Horm. Behav. 103 (2018), 80–96.
Smith, G.T., Brenowitz, E.A., Beecher, M.D., Wingfield, J.C., Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J. Neurosci. 17 (1997), 6001–6010.
Stevenson, T.J., Bernard, D.J., McCarthy, M.M., Ball, G.F., Photoperiod-dependent regulation of gonadotropin-releasing hormone 1 messenger ribonucleic acid levels in the songbird brain. Gen. Comp. Endocrinol. 190 (2013), 81–87.
Stokes, T.M., Leonard, C.M., Nottebohm, F., The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J. Comp. Neurol. 156 (1974), 337–374.
Storey, C.R., Nicholls, T.J., Some effects of manipulation of daily photoperiod on the rate of onset of a photorefractory state in canaries (Serinus canarius). Gen. Comp. Endocrinol. 30 (1976), 204–208.
Storey, C.R., Nicholls, T.J., Follett, B.K., Castration accelerates the rate of onset of photorefractoriness in the canary (Serinus canarius). Gen. Comp. Endocrinol. 42 (1980), 315–319.
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.
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.
Tramontin, A.D., Wingfield, J.C., Brenowitz, P.A., Contributions of social cues and photoperiod to seasonal plasticity in the adult avian song control system. J. Neurosci. 19 (1999), 476–483.
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., Perfito, N., Wingfield, J.C., Brenowitz, E.A., Seasonal growth of song control nuclei precedes seasonal reproductive development in wild adult song sparrows. Gen. Comp. Endocrinol. 122 (2001), 1–9.
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.
Vandries, L.M., Ghorbanpoor, S., Cornez, G., Shevchouk, O.T., Ball, G.F., Cornil, C.A., Balthazart, J., Testosterone or estradiol when implanted in the medial preoptic nucleus trigger short low-amplitude songs in female canaries. eNeuro, 2019, 6.
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.
Williams, T.D., Dawson, A., Nicholls, T.J., Goldsmith, A.R., Short days induce premature reproductive maturation in juvenile starlings, Sturnus vulgaris. J. Reprod. Fertil. 80 (1987), 327–333.
Wingfield, J.C., Farner, D.S., The annual cycle of plasma irLH and steroid hormones in feral populations of the white-crowned sparrow, Zonotrichia leucophrys gambelii. Biol. Reprod. 19 (1978), 1046–1056.
Wingfield, J.C., Moore, M.C., Hormonal, social, and environmental factors in the reproductive biology of free-living male birds. Crews, D., (eds.) Psychobiology of Reproductive Behavior: An Evolutionary Perspective, 1987, Prentice-Hall, Englewood Cliffs NJ, 148–175.
Wingfield, J.C., Hegner, R.E., Dufty, A.M., Ball, G.F., The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems and breedings strategies. Am. Nat. 136 (1990), 829–846.
Wingfield, J.C., Jacobs, J., Hillgarth, N., Ecological constraints and the evolution of hormone-behavior interrelationships. Ann. NY Acad. Sci. 807 (1997), 22–41.
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.