The neural distribution of the avian homologue of oxytocin, mesotocin, in two songbird species, the zebra finch and the canary: A potential role in song perception and production.
Haakenson, Chelsea M; Balthazart, Jacques; Madison, Farrah Net al.
2022 • In Journal of Comparative Neurology, 530 (13), p. 2402 - 2414
[en] The avian homologue of oxytocin (OT), formerly called mesotocin, influences social behaviors in songbirds and potentially song production. We sought to characterize the distribution of OT peptide in the brain of two songbird species: canaries (Serinus canaria) and zebra finches (Taeniopygia guttata). To visualize OT, we performed immunocytochemistry using an antibody previously shown to identify OT in avian species. In both canaries and zebra finches, dense OT-ir perikarya were located in the paraventricular nucleus (PVN), preoptic area (POA), supraoptic nucleus (SON), and medial bed nucleus of the stria terminalis (BNSTm). We also observed morphologically distinct OT-ir cells scattered throughout the mesopallium. OT-ir fibers were observed in the PVN, ventral medial hypothalamus (VMH), periaqueductal gray (PAG), intercollicular nucleus (ICo), and ventral tegmental area (VTA). We also observed punctate OT-ir fibers in the song control nucleus HVC. In both male and female canaries, OT-ir fibers were present in the lateral septum (LS), but innervation was greater in males. We did not observe this sex difference in zebra finches. Much of the OT staining observed is consistent with general distributions within the vertebrate hypothalamus, indicating a possible conserved function. However, some extra-hypothalamic distributions, such as perikarya in the mesopallium, may be specific to songbirds and play a role in song perception and production. The presence of OT-ir fibers in HVC and song control nuclei projecting dopaminergic regions provides anatomical evidence in support of the idea that OT can influence singing behavior-either directly via HVC or indirectly via the PAG, VTA, or POA.
Disciplines :
Zoology
Author, co-author :
Haakenson, Chelsea M ; Program in Neuroscience and Cognitive Science, Department of Psychology, University of Maryland, College Park, Maryland, USA
Balthazart, Jacques ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Madison, Farrah N; Program in Neuroscience and Cognitive Science, Department of Psychology, University of Maryland, College Park, Maryland, USA ; Department of Biology, Hope College, Holland, Michigan, USA
Ball, Gregory F; Program in Neuroscience and Cognitive Science, Department of Psychology, University of Maryland, College Park, Maryland, USA
Language :
English
Title :
The neural distribution of the avian homologue of oxytocin, mesotocin, in two songbird species, the zebra finch and the canary: A potential role in song perception and production.
NINDS - National Institute of Neurological Disorders and Stroke
Funding text :
We acknowledge the Imaging Core Facility in the department of Cell Biology and Molecular Genetics at the University of Maryland, College Park for use of the Nikon Eclipse microscope and software. This work was supported by NINDS 1 R01 NS104008‐01.
Acher, R. (1993). Neurohypophysial peptide systems: Processing machinery, hydroosmotic regulation, adaptation and evolution. Regulatory Peptides, 45(1–2), 1–13. https://doi.org/10.1016/0167-0115(93)90174-7
Alger, S. J., Maasch, S. N., & Riters, L. V. (2009). Lesions to the medial preoptic nucleus affect immediate early gene immunolabeling in brain regions involved in song control and social behavior in male European starlings. European Journal of Neuroscience, 29(5), 970–982. https://doi.org/10.1111/j.1460-9568.2009.06637.x
Alward, B. A., Balthazart, J., & Ball, G. F. (2013). Differential effects of global versus local testosterone on singing behavior and its underlying neural substrate. Proceedings of the National Academy of Sciences of the United States of America, 110(48), 19573–19578. https://doi.org/10.1073/pnas.1311371110
Appeltants, D., Absil, P., Balthazart, J., & Ball, G. F. (2000). Identification of the origin of catecholaminergic inputs to HVc in canaries by retrograde tract tracing combined with tyrosine hydroxylase immunocytochemistry. Journal of Chemical Neuroanatomy, 18(3), 117–133. https://doi.org/10.1016/S0891-0618(99)00054-X
Appeltants, D., Ball, G. F., & Balthazart, J. (2002). The origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport, 13(5), 649–653. https://doi.org/10.1097/00001756-200204160-00023
Aste, N., Balthazart, J., Absil, P., Grossmann, R., Mülhbauer, E., Viglietti-Panzica, C., & Panzica, G. C. (1998). Anatomical and neurochemical definition of the nucleus of the stria terminalis in Japanese quail (Coturnix japonica). Journal of Comparative Neurology, 396(2), 141–157. https://doi.org/10.1002/(SICI)1096-9861(19980629)396:2<141::AID-CNE1>3.0.CO;2-0
Balthazart, J., Absil, P., Foidart, A., Houbart, M., Harada, N., & Ball, G. F. (1996). 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. Journal of Neurobiology, 31(2), 129–148. https://doi.org/10.1002/(SICI)1097-4695(199610)31:2<129::AID-NEU1>3.0.CO;2-D
Baran, N. M., Peck, S. C., Kim, T. H., Goldstein, M. H., & Adkins-regan, E. (2017). Early life manipulations of vasopressin-family peptides alter vocal learning. Proceedings of the Royal Society B: Biological Sciences, 284, 20171114.
Barth, S. W., Bathgate, R. A. D., Mess, A., Parry, L. J., Ivell, R., & Grossmann, R. (1997). Mesotocin gene expression in the diencephalon of domestic fowl: Cloning and sequencing of the MT cDNA and distribution of MT gene expressing neurons in the chicken hypothalamus. Journal of Neuroendocrinology, 9(10), 777–787. https://doi.org/10.1046/j.1365-2826.1997.00643.x
Beecher, M. D., & Burt, J. M. (2004). The role of social interaction in bird song learning. Current Directions in Psychological Science, 13(6), 224–228. https://doi.org/10.1111/j.0963-7214.2004.00313.x
Ben-Tov, M., Duarte, F., & Mooney, R. (2021). A neural hub that coordinates learned and innate courtship behaviors. bioRxiv, 2021.09.09.459618.
Bons, N. (1980). The topography of mesotocin and vasotocin systems in the brain of the domestic mallard and japanese quail: Immunocytochemical identification. Cell And Tissue Research, 213(1), 37–51. https://doi.org/10.1007/BF00236919
Bons, N. (1983). Immunocytochemical identification of the mesotocin- and vasotocin-producing systems in the brain of temperate and desert lizard species and their modifications by cold exposure. General and Comparative Endocrinology, 52(1), 56–66. https://doi.org/10.1016/0016-6480(83)90158-2
Buijs, R. M., Swaab, D. F., Dogterom, J., & van Leeuwen, F. W. (1978). Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Cell and Tissue Research, 186, 423–433.
Caffé, A. R., Van Ryen, P. C., Van Der Woude, T. P., & Van Leeuwen, F. W. (1989). Vasopressin and oxytocin systems in the brain and upper spinal cord of Macaca fascicularis. Journal of Comparative Neurology, 287(3), 302–325. https://doi.org/10.1002/cne.902870304
Carouso-Peck, S., Menyhart, O., DeVoogd, T. J., & Goldstein, M. H. (2020). Contingent parental responses are naturally associated with zebra finch song learning. Animal Behaviour, 165, 123–132. https://doi.org/10.1016/j.anbehav.2020.04.019
Castelino, C. B., Diekamp, B., & Ball, G. F. (2007). Noradrenergic projections to the song control nucleus area X of the medial striatum in male zebra finches (Taeniopygia guttata). Journal of Comparative Neurology, 502, 544–562. https://doi.org/10.1002/cne
Catchpole, C. K., & Slater, P. J. B. (2008). Bird song: Biological themes and variations (2nd ed.). Cambridge University Press. https://doi.org/10.1017/CBO9780511754791
Charlet, A., & Grinevich, V. (2017). Oxytocin mobilizes midbrain dopamine toward sociality. Neuron, 95, 235–237.
Chen, Y., Matheson, L. E., & Sakata, J. T. (2016). Mechanisms underlying the social enhancement of vocal learning in songbirds. Proceedings of the National Academy of Sciences, 113(24), 6641–6646. https://doi.org/10.1073/pnas.1522306113
Chokchaloemwong, D., Prakobsaeng, N., Sartsoongnoen, N., Kosonsiriluk, S., El Halawani, M., & Chaiseha, Y. (2013). Mesotocin and maternal care of chicks in native Thai hens (Gallus domesticus). Hormones and Behavior, 64(1), 53–69. https://doi.org/10.1016/j.yhbeh.2013.04.010
Davis, M. T., Grogan, K. E., Fraccaroli, I., Libecap, T. J., Natalie, R., & Maney, D. L. (2022). Expression of oxytocin receptors in the zebra finch brain during vocal development. Developmental Neurobiology, 82(1), 3–15. https://doi.org/10.1002/dneu.22851.Expression
de Jong, T. R., & Neumann, I. D. (2018). Oxytocin and aggression. Behavioral Pharmacology of Neuropeptides, 35, 175–192. https://doi.org/10.1007/7854_2017_13
De Vries, G. J., & Buijs, R. M. (1983). The origin of the vasopressinergic and oxytocinergic innervation of the rat brain with special reference to the lateral septum. Brain Research, 273, 307–317.
Duque, J. F., Leichner, W., Ahmann, H., & Stevens, J. R. (2018). Mesotocin influences pinyon jay prosociality. Biology Letters, 14(4), 20180105. https://doi.org/10.1098/rsbl.2018.0105
Floody, O. R., Cooper, T. T., & Albers, H. E. (1998). Injection of oxytocin into the medial preoptic-anterior hypothalamus increases ultrasound production by female hamsters. Peptides, 19(5), 833–839. https://doi.org/10.1016/S0196-9781(98)00029-1
Follett, B. K., Hinde, R. A., Steel, E., & Nicholls, T. J. (1973). The influence of photoperiod on nest building, ovarian development and luteinizing hormone secretion in canaries (Serinus canarius). Journal of Endocrinology, 59(1), 151–162. https://doi.org/10.1677/joe.0.0590151
Froemke, R. C., & Young, L. J. (2021). Oxytocin, neural plasticity, and social behavior. Annual Review of Neuroscience, 44, 359–381.
Goodson, J. L., Evans, A. K., & Bass, A. H. (2003). Putative isotocin distributions in sonic fish: Relation to vasotocin and vocal-acoustic circuitry. Journal of Comparative Neurology, 462(1), 1–14. https://doi.org/10.1002/cne.10679
Goodson, J. L., Schrock, S. E., & Kingsbury, M. A. (2015). Oxytocin mechanisms of stress response and aggression in a territorial finch. Physiology and Behavior, 141, 154–163. https://doi.org/10.1016/j.physbeh.2015.01.016
Goodson, J. L., Schrock, S. E., Klatt, J. D., Kabelik, D., & Kingsbury, M. A. (2009). Mesotocin and nonapeptide receptors promote estrildid flocking behavior. Science, 325(5942), 862–866. https://doi.org/10.1126/science.1174929
Goossens, N., Blähser, S., Oksche, A., Vandesande, F., & Dierickx, K. (1977). Immunocytochemical investigation of the hypothalamo-neurohypophysial system in birds. Cell and Tissue Research, 184(1), 1–13. https://doi.org/10.1007/BF00220523
Gordon, I., Martin, C., Feldman, R., & Leckman, J. F. (2011). Oxytocin and social motivation. Developmental Cognitive Neuroscience, 1, 471–493.
Haakenson, C. M., Balthazart, J., & Ball, G. F. (2020). Effects of inactivation of the periaqueductal gray on song production in testosterone-treated male canaries (Serinus canaria). Eneuro, 7(4), ENEURO. https://doi.org/10.1523/eneuro.0048-20.2020
Hara, E., Kubikova, L., Hessler, N. A., & Jarvis, E. D. (2007). Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context. European Journal of Neuroscience, 25(11), 3406–3416. https://doi.org/10.1111/j.1460-9568.2007.05600.x
He, Z., Zhang, L., Hou, W., Zhang, X., Young, L. J., Li, L., Liu, L., Ma, H., Xun, Y., Lv, Z., Li, Y., Jia, R., Li, J., & Tai, F. (2021). Paraventricular nucleus oxytocin subsystems promote active paternal behaviors in Mandarin voles. Journal of Neuroscience, 41(31), 6699–6713. https://doi.org/10.1523/JNEUROSCI.2864-20.2021
Heimovics, S. A., Salvante, K. G., Sockman, K. W., & Riters, L. V. (2011). Individual differences in the motivation to communicate relate to levels of midbrain and striatal catecholamine markers in male European starlings. Hormones and Behavior, 60(5), 529–539. https://doi.org/10.1016/j.yhbeh.2011.08.001
Hermes, M. L. H. J., Buijs, R. M., Masson-Pévet, M., & Pévet, P. (1988). Oxytocinergic innervation of the brain of the garden dormouse (Eliomys quercinus L.). Journal of Comparative Neurology, 273(2), 252–262. https://doi.org/10.1002/cne.902730209
Insel, T. R., & Shapiro, L. E. (1992). Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proceedings of the National Academy of Sciences of the United States of America, 89(13), 5981–5985. https://doi.org/10.1073/pnas.89.13.5981
Insel, T. R., & Winslow, J. T. (1991). Central administration of oxytocin modulates the infant rats response to social isolation. European Journal of Pharmacology, 203(1), 149–152. https://doi.org/10.1016/0014-2999(91)90806-2
Jiang, W. Q., Bao, L. L., Sun, F. J., Liu, X. L., & Yang, J. (2019). Oxytocin in the periaqueductal gray mainly comes form the hypothalamic supraoptic nucleus to participate in pain modulation. Peptides, 121(July), 170153. https://doi.org/10.1016/j.peptides.2019.170153
Karten, H. J., & Hodos, W. (1967). Stereotaxic atlas of the brain of the pigeon (Columba livia). The Auk, 86, 152–153.
Kelly, A. M., & Goodson, J. L. (2014). Hypothalamic oxytocin and vasopressin neurons exert sex-specific effects on pair bonding, gregariousness, and aggression in finches. Proceedings of the National Academy of Sciences, 111(16), 6069–6074. https://doi.org/10.1073/pnas.1322554111
King, A. P., & West, M. J. (1988). Searching for the functional origins of song in eastern brown-headed cowbirds, Molothrus ater ater. Animal Behaviour, 36(6), 1575–1588. https://doi.org/10.1016/S0003-3472(88)80100-3
Koussounadis, A., Langdon, S. P., Um, I. H., Harrison, D. J., & Smith, V. A. (2015). Relationship between differentially expressed mRNA and mRNA-protein correlations in a xenograft model system. Scientific Reports, 5(June), 1–9. https://doi.org/10.1038/srep10775
Kuenzel, W. J., & Masson, M. (1988). A stereotaxic atlas of the brain of the chick (Gallus domesticus). The Johns Hopkins University Press.
Leung, C. H., Abebe, D. F., Earp, S. E., Goode, C. T., Grozhik, A. V., Mididoddi, P., & Maney, D. L. (2011). Neural distribution of vasotocin receptor mRNA in two species of songbird. Endocrinology, 152(12), 4865–4881. https://doi.org/10.1210/en.2011-1394
Lewis, J. W., Ryan, S. M., Arnold, A. P., & Butcher, L. L. (1981). Evidence for a catecholaminergic projection to area X in the zebra finch. The Journal of Comparative Neurology, 196(2), 347–354. https://doi.org/10.1002/cne.901960212
Liu, Y., & Wang, Z. X. (2003). Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience, 121(3), 537–544. https://doi.org/10.1016/S0306-4522(03)00555-4
Love, T. M. (2014). Oxytocin, motivation and the role of dopamine. Pharmacology, Biochemistry and Behavior, 119, 49–60. https://doi.org/10.1016/j.pbb.2013.06.011
Lynch, K. S., Diekamp, B., & Ball, G. F. (2008). Catecholaminergic cell groups and vocal communication in male songbirds. Physiology and Behavior, 93(4–5), 870–876. https://doi.org/10.1016/j.physbeh.2007.12.004
Maier, T., Güell, M., & Serrano, L. (2009). Correlation of mRNA and protein in complex biological samples. FEBS Letters, 583, 3966–3973. https://doi.org/10.1016/j.febslet.2009.10.036
Maney, D. L., & Rodriguez-Saltos, C. A. (2016). Hormones and the incentive salience of bird song. In A. Bass, J. Sisneros, A. Popper, & R. Fay, (Eds.), Hearing and hormones. Springer handbook of auditory research (pp. 101–132). Springer. https://doi.org/10.1007/978-3-319-26597-1_5
Meddle, S. (2021, July 2). Neuroendocrine regulation of avian parental behaviour. In Simone Meddle & Oliver Bosch (Chairs) Neuroendocrine regulation of parental behavior - A comparative perspective [Symposium]. Society for Behavioral Neuroendocrinology, Virtual.
Melis, M. R., Melis, T., Cocco, C., Succu, S., Sanna, F., Pillolla, G., Boi, A., Ferri, G.-L., & Argiolas, A. (2007). Oxytocin injected into the ventral tegmental area induces penile erection and increases extracellular dopamine in the nucleus accumbens and paraventricular nucleus of the hypothalamus of male rats. European Journal of Neuroscience, 26(4), 1026–1035. https://doi.org/10.1111/j.1460-9568.2007.05721.x
Nelson, D. A., & Marler, P. (1994). Selection-based learning in bird song development. Proceedings of the National Academy of Sciences of the United States of America, 91(22), 10498–10501. https://doi.org/10.1073/pnas.91.22.10498
Nieder, A., & Mooney, R. (2020). The neurobiology of innate, volitional and learned vocalizations in mammals and birds. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 375(1789), 20190054. https://doi.org/10.1098/rstb.2019.0054
Pedersen, A., & Tomaszycki, M. L. (2012). Oxytocin antagonist treatments alter the formation of pair relationships in zebra finches of both sexes. Hormones and Behavior, 62(2), 113–119. https://doi.org/10.1016/j.yhbeh.2012.05.009
Pilgeram, N. R., Baran, N. M., Bhise, A., Davis, M. T., Kim, E., Lee, S., Rodriguez-Saltos, C. A., & Maney, D. L. (2021). Oxytocin receptor antagonism during song tutoring in zebra finches reduces preference for and learning of the tutor's song. bioRxiv, https://doi.org/10.1101/2021.06.16.448133
Puelles, L., Martinez-de-la-Torre, M., Martinez, S., Watson, C., & Paxinos, G. (2018). The chick brain in stereotaxic coordinates and alternate stains: Featuring neuromeric divisions and mammalian homologies. Academic Press.
Reiner, A., Perkel, D. J., Bruce, L. L., Butler, A. B., Csillag, A., Kuenzel, W., Medina, L., Paxinos, G., Shimizu, T., Striedter, G., Wild, M., Ball, G. F., Durand, S., Gütürkün, O., Lee, D. W., Mello, C. V., Powers, A., White, S. A., Hough, G., & Kubikova, L. (2004). Revised nomenclature for avian telencephalon and some related brainstem nuclei. Journal of Comparative Neurology, 473(3), 377–414. https://doi.org/10.1002/cne.20118
Reiner, A., Perkel, D. J., Mello, C. V., & Jarvis, E. D. (2004). Songbirds and the revised avian brain nomenclature. Annals of the New York Academy of Sciences, 5, 77–108.
Riters, L. V., & Alger, S. J. (2004). Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: Possible neural substrates for sexually motivated song. Cell and Tissue Research, 316(1), 35–44. https://doi.org/10.1007/s00441-003-0838-6
Romero, T., Nagasawa, M., Mogi, K., Hasegawa, T., & Kikusui, T. (2014). Oxytocin promotes social bonding in dogs. Proceedings of the National Academy of Sciences of the United States of America, 111(25), 9085–9090. https://doi.org/10.1073/pnas.1322868111
Ross, H. E., & Young, L. J. (2009). Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Frontiers in Neuroendocrinology, 30(4), 534–547. https://doi.org/10.1016/j.yfrne.2009.05.004
Saayman, H. S., Naude, R. J., Oelofsen, W., & Isaacson, L. C. (1986). Mesotocin and vasotocin, two neurohypophysial hormones in the ostrich, Struthio camelus. International Journal of Peptide and Protein Research, 28(4), 398–402. https://doi.org/10.1111/j.1399-3011.1986.tb03271.x
Sakata, J. T., & Brainard, M. S. (2009). Social context rapidly modulates the influence of auditory feedback on avian vocal motor control. Journal of Neurophysiology, 102(4), 2485–2497. https://doi.org/10.1152/jn.00340.2009
Sakata, J. T., Hampton, C. M., & Brainard, M. S. (2008). Social modulation of sequence and syllable variability in adult birdsong. Journal of Neurophysiology, 99(4), 1700–1711. https://doi.org/10.1152/jn.01296.2007
Sawyer, W. H. (1977). Evolution of active neurohypophysial principles among the vertebrates. American Zoologist, 17(4), 727–737. https://doi.org/10.1093/icb/17.4.727
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. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676–682. https://doi.org/10.1038/nmeth.2019
Shamay-Tsoory, S. G., & Abu-Akel, A. (2016). The social salience hypothesis of oxytocin. Biological Psychiatry, 79(3), 194–202. https://doi.org/10.1016/j.biopsych.2015.07.020
Silveira, P. F., Breno, M. C., Martín Del Río, M. P., & Mancera, J. M. (2002). The distribution of vasotocin and mesotocin immunoreactivity in the brain of the snake, Bothrops jararaca. Journal of Chemical Neuroanatomy, 24(1), 15–26. https://doi.org/10.1016/S0891-0618(02)00016-9
Sinpru, P., Porter, T. E., El Halawani, M. E., & Chaiseha, Y. (2017). Effects of nest-deprivation on hypothalamic mesotocin in incubating native Thai hens (Gallus domesticus). Acta Histochemica, 119(7), 708–718. https://doi.org/10.1016/j.acthis.2017.09.002
Smeets, W. J. A. J., & González, A. (2001). Vasotocin and mesotocin in the brains of amphibians: State of the art. Microscopy Research and Technique, 54(3), 125–136. https://doi.org/10.1002/jemt.1128
Smith, A. S., Ågmo, A., Birnie, A. K., & French, J. A. (2010). Manipulation of the oxytocin system alters social behavior and attraction in pair-bonding primates, Callithrix penicillata. Hormones and Behavior, 57(2), 255–262. https://doi.org/10.1016/j.yhbeh.2009.12.004
Sofroniew, M. V., Weindl, A., Schinko, I., & Wetzstein, R. (1979). The distribution of vasopressin-, oxytocin-, and neurophysin-producing neurons in the guinea pig brain. I. The classical hypothalamo-neurohypophyseal system. Cell and Tissue Research, 196(3), 367–384. https://doi.org/10.1007/BF00234734
Steel, E., & Hinde, R. A. (2009). Effect of artificially increased day length in winter on female domesticated canaries. Journal of Zoology, 149(1), 1–11. https://doi.org/10.1111/j.1469-7998.1966.tb02977.x
Stokes, T. M., Leonard, C. M., & Nottebohm, F. (1974). The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. Journal of Comparative Neurology, 156(3), 337–374. https://doi.org/10.1002/cne.901560305
Succu, S., Sanna, F., Cocco, C., Melis, T., Boi, A., Ferri, G.-L., Argiolas, A., & Melis, M. R. (2008). Oxytocin induces penile erection when injected into the ventral tegmental area of male rats: Role of nitric oxide and cyclic GMP. European Journal of Neuroscience, 28(4), 813–821. https://doi.org/10.1111/j.1460-9568.2008.06385.x
Succu, S., Sanna, F., Melis, T., Boi, A., Argiolas, A., & Melis, M. R. (2007). Stimulation of dopamine receptors in the paraventricular nucleus of the hypothalamus of male rats induces penile erection and increases extra-cellular dopamine in the nucleus accumbens: Involvement of central oxytocin. Neuropharmacology, 52(3), 1034–1043. https://doi.org/10.1016/j.neuropharm.2006.10.019
Tanaka, M., Sun, F., Li, Y., & Mooney, R. (2018). A mesocortical dopamine circuit enables the cultural transmission of vocal behavior. Nature, 563, 117–120.
Thayananuphat, A., Youngren, O. M., Kang, S. W., Bakken, T., Kosonsiriluk, S., Chaiseha, Y., & El Halawani, M. E. (2011). Dopamine and mesotocin neurotransmission during the transition from incubation to brooding in the turkey. Hormones and Behavior, 60(4), 327–335. https://doi.org/10.1016/j.yhbeh.2011.06.009
Theofanopoulou, C., Boeckx, C., & Jarvis, E. D. (2017). A hypothesis on a role of oxytocin in the social mechanisms of speech and vocal learning. Proceedings of the Royal Society B: Biological Sciences, 284(1861), 20170988. https://doi.org/10.1098/rspb.2017.0988
Theofanopoulou, C., Gedman, G., Cahill, J. A., Boeckx, C., & Jarvis, E. D. (2021). Universal nomenclature for oxytocin–vasotocin ligand and receptor families. Nature, 592(7856), 747–755. https://doi.org/10.1038/s41586-020-03040-7
Thepen, T., Voorn, P., Stoll, C. J., Sluiter, A. A., Pool, C. W., & Lohman, A. H. M. (1987). Mesotocin and vasotocin in the brain of the lizard Gekko gecko. Cell and Tissue Research, 250, 649–656.
Tobari, Y., Theofanopoulou, C., Mori, C., Sato, Y., Marutani, M., Fujioka, S., Konno, N., Suzuki, K., Furutani, A., Hakataya, S., Yao, C.-T., Yang, E.-Y., Tsai, C.-R., Tang, P.-C., Chen, C.-F., Boeckx, C., Jarvis, E. D., & Okanoya, K. (2022). Oxytocin variation and brain region-specific gene expression in a domesticated avian species. Genes, Brain and Behavior, 21(2), 1–15. https://doi.org/10.1111/gbb.12780
Tomaszycki, M. L., & Adkins-Regan, E. (2005). Experimental alteration of male song quality and output affects female mate choice and pair bond formation in zebra finches. Animal Behaviour, 70(4), 785–794. https://doi.org/10.1016/j.anbehav.2005.01.010
Tops, M., van Ijzendoorn, M. H., Riem, M. M. E., Boksem, M. A. S., & Bakermans-Kranenburg, M. J. (2011). Oxytocin receptor gene associated with the efficiency of social auditory processing. Frontiers in Psychiatry, 2(Nov), 1–4. https://doi.org/10.3389/fpsyt.2011.00060
Vaccari, C., Lolait, S. J., & Ostrowski, N. L. (1998). Comparative distribution of vasopressin V1b and oxytocin receptor messenger ribonucleic acids in brain. Endocrinology, 139(12), 5015–5033.
Vicario, A., Mendoza, E., Abellán, A., Scharff, C., & Medina, L. (2017). Genoarchitecture of the extended amygdala in zebra finch, and expression of FoxP2 in cell corridors of different genetic profile. Brain Structure and Function, 222, 481–514. https://doi.org/10.1007/s00429-016-1229-6
Vogel, C., & Marcotte, E. M. (2012). Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nature Reviews Genetics, 13(4), 227–232. https://doi.org/10.1038/nrg3185
West, M. J., & King, A. P. (1988). Female visual displays affect the development of male song in the cowbird. Nature, 334(6179), 244–246. https://doi.org/10.1038/334244a0
Winslow, J. T., & Insel, T. R. (1991). Social status in pairs of male squirrel monkeys determines the behavioral response to central oxytocin administration. Journal of Neuroscience, 11(7), 2032–2038. https://doi.org/10.1523/jneurosci.11-07-02032.1991
Winslow, J. T., Hearn, E. F., Ferguson, J., Young, L. J., Matzuk, M. M., & Insel, T. R. (2000). Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse. Hormones and Behavior, 37, 145–155. https://doi.org/10.1006/hbeh.1999.1566
Young, L. J. (1999). Oxytocin and vasopressin receptors and species-typical social behaviors. Hormones and Behavior, 36, 212–221. https://doi.org/10.1006/hbeh.1999.1548
Zann, R. A. (1996). The zebra finch: A synthesis of laboratory and field studies. Oxford University Press.
Zebra Finch Expression Brain Atlas (ZEBrA). Portland, OR 97239: Oregon Health & Science University http://www.zebrafinchatlas.org
