Seasonal and individual variation in singing behavior correlates with alpha 2-noradrenergic receptor density in brain regions implicated in song, sexual, and social behavior

Neuroscience

Volumn 182, Issue , 2011, Pages 133-143

  Heimovics, S A ^a,d   Cornil, C A ^b,c   Ellis, J M S ^a   Ball, G F ^c   Riters, L V ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Communication; Motivation; Norepinephrine; Seasonality; Social behavior; Song control system

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; NORADRENALIN; TESTOSTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTUMN; BRAIN FUNCTION; BRAIN NUCLEUS; CONTROLLED STUDY; FEMALE; MALE; NEUROANATOMY; NONHUMAN; PREOPTIC NUCLEUS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; SEASONAL VARIATION; SEXUAL AROUSAL; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SONGBIRD; SPRING;

ANIMALS; BRAIN; BRAIN MAPPING; FEMALE; MALE; NOREPINEPHRINE; RECEPTORS, ADRENERGIC, ALPHA-2; SEASONS; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; STARLINGS; VOCALIZATION, ANIMAL;

EID: 79955476790     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.03.012     Document Type: Article

References (88)

1. Alger S.J., Maasch S.N., Riters L.V. 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. Eur J Neurosci 2009, 29:970-982.
2. Alger S.J., Riters L.V. Lesions to the medial preoptic nucleus differentially affect singing and nest box-directed behaviors within and outside of the breeding season in European starlings (Sturnus vulgaris). Behav Neurosci 2006, 120:1326-1336.
3. Aston-Jones G., Cohen J.D. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 2005, 28:403-450.
4. Bailhache T., Surlemont C., Balthazart J. Effects of neurochemical lesions of the preoptic area on male sexual behavior in the Japanese quail. Brain Res Bull 1993, 32:273-283.
5. Ball G.F., Auger C.J., Bernard D.J., Charlier T.D., Sartor J.J., Riters L.V., Balthazart J. Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann N Y Acad Sci 2004, 1016:586-610.
6. Ball G.F., Balthazart J. Steroid modulation of muscarinic cholinergic and alpha2-adrenergic receptor density in the nucleus intercollicularis of the Japanese quail. Eur J Neurosci 1990, 2:828-835.
7. Ball G.F., Balthazart J. Individual variation and the endocrine regulation of behaviour and physiology in birds: a cellular/molecular perspective. Philos Trans R Soc Lond B Biol Sci 2008, 363:1699-1710.
8. Ball GF, Balthazart J (in press) Sexual arousal, is it for mammals only? Horm Behav, in press.
9. 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. Neuroscience of birdsong 2008, 320-331. Cambridge University Press, Cambridge. H.P. Ziegler, P.R. Marler (Eds.).
10. Balthazart J., Absil P., Gerard M., Appeltants D., Ball G.F. Appetitive and consummatory male sexual behavior in Japanese quail are differentially regulated by subregions of the preoptic medial nucleus. J Neurosci 1998, 18:6512-6527.
11. Balthazart J., Ball G.F. Effects of the noradrenergic neurotoxin DSP-4 on luteinizing hormone levels, catecholamine concentrations, alpha 2-adrenergic receptor binding, and aromatase activity in the brain of the Japanese quail. Brain Res 1989, 492:163-175.
12. Balthazart J., Ball G.F. Topography in the preoptic region: differential regulation of appetitive and consummatory male sexual behaviors. Front Neuroendocrinol 2007, 28:161-178.
13. Barclay S.R., Harding C.F. Androstenedione modulation of monoamine levels and turnover in hypothalamic and vocal control nuclei in the male zebra finch: steroid effects on brain monoamines. Brain Res 1988, 459:333-343.
14. Barclay S.R., Harding C.F. Differential modulation of monoamine levels and turnover rates by estrogen and/or androgen in hypothalamic and vocal control nuclei of male zebra finches. Brain Res 1990, 523:251-262.
15. Barclay S.R., Harding C.F., Waterman S.A. Correlations between catecholamine levels and sexual behavior in male zebra finches. Pharmacol Biochem Behav 1992, 41:195-201.
16. Barclay S.R., Harding C.F., Waterman S.A. Central DSP-4 treatment decreases norepinephrine levels and courtship behavior in male zebra finches. Pharmacol Biochem Behav 1996, 53:213-220.
17. Bernard D.J., Ball G.F. Two histological markers reveal a similar photoperiodic difference in the volume of the high vocal center in male European starlings. J Comp Neurol 1995, 360:726-734.
18. Berridge C.W., Waterhouse B.D. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 2003, 42:33-84.
19. Brainard M.S. The anterior forebrain pathway and vocal plasticity. Neuroscience of birdsong 2008, 240-255. Cambridge University Press, Cambridge. H.P. Ziegler, P.R. Marler (Eds.).
20. Brenowitz E.A. Plasticity of the adult avian song control system. Ann N Y Acad Sci 2004, 1016:560-585.
21. Brenowitz E.A. Plasticity of the song control system in adult birds. Neuroscience of birdsong 2008, 332-349. Cambridge University Press, Cambridge. H.P. Ziegler, P.R. Marler (Eds.).
22. Cardin J.A., Schmidt M.F. Noradrenergic inputs mediate state dependence of auditory responses in the avian song system. J Neurosci 2004, 24:7745-7753.
23. Caro S.P., Lambrechts M.M., Balthazart J. Early seasonal development of brain song control nuclei in male blue tits. Neurosci Lett 2005, 386:139-144.
24. Castelino C.B., Ball G.F. A role for norepinephrine in the regulation of context-dependent ZENK expression in male zebra finches (Taeniopygia guttata). Eur J Neurosci 2005, 21:1962-1972.
25. Castelino C.B., Schmidt M.F. What birdsong can teach us about the central noradrenergic system. J Chem Neuroanat 2010, 39:96-111.
26. Catchpole C.K., Slater P.J.B. Bird song: biological themes and variations 2008, Cambridge University Press, Cambridge, [England].
27. Chen F., Lawrence A.J. The effects of antidepressant treatment on serotonergic and dopaminergic systems in Fawn-Hooded rats: a quantitative autoradiography study. Brain Res 2003, 976:22-29.
28. Cornil C.A., Ball G.F. Interplay among catecholamine systems: dopamine binds to alpha2-adrenergic receptors in birds and mammals. J Comp Neurol 2008, 511:610-627.
29. Crews D. Evolution of neuroendocrine mechanisms that regulate sexual behavior. Trends Endocrinol Metab 2005, 16:354-361.
30. Dawson A., King V.M., Bentley G.E., Ball G.F. Photoperiodic control of seasonality in birds. J Biol Rhythms 2001, 16:365-380.
31. Diez-Alarcia R., Pilar-Cuellar F., Paniagua M.A., Meana J.J., Fernandez-Lopez A. Pharmacological characterization and autoradiographic distribution of alpha2-adrenoceptor antagonist [3H]RX 821002 binding sites in the chicken brain. Neuroscience 2006, 141:357-369.
32. Dloniak S.M., Deviche P. Effects of testosterone and photoperiodic condition on song production and vocal control region volumes in adult male dark-eyed juncos (Junco hyemalis). Horm Behav 2001, 39:95-105.
33. Duckworth R.A. Evolution of personality: developmental constraints on behavioral flexibility. Auk 2010, 127:752-758.
34. Eens M. Understanding the complex song of the European starling: an integrated approach. Adv Study Behav 1997, 26:355-434.
35. Feare C.J. The Starling 1984, Oxford Press, Oxford.
36. Gahr M. Distribution of sex steroid hormone receptors in the avian brain: functional implications for neural sex differences and sexual behaviors. Microsc Res Tech 2001, 55:1-11.
37. Gentner T.Q. Temporal auditory pattern recognition in songbirds. Neuroscience of Birdsong 2008, 187-198. Cambridge University Press, Cambridge. H.P. Ziegler, P.R. Marler (Eds.).
38. Gil D., Bulmer E., Celis P., Puerta M. Increased sibling competition does not increase testosterone or corticosterone levels in nestlings of the spotless starling (Sturnus unicolor). Horm Behav 2008, 54:238-243.
39. Goodson J.L. The vertebrate social behavior network: evolutionary themes and variations. Horm Behav 2005, 48:11-22.
40. Goodson J.L., Eibach R., Sakata J., Adkins-Regan E. Effect of septal lesions on male song and aggression in the colonial zebra finch (Taeniopygia guttata) and the territorial field sparrow (Spizella pusilla). Behav Brain Res 1999, 101:167-180.
41. Gulia K.K., Kumar V.M., Mallick H.N. Role of the lateral septal noradrenergic system in the elaboration of male sexual behavior in rats. Pharmacol Biochem Behav 2002, 72:817-823.
42. Halme M., Sjoholm B., Savola J.M., Scheinin M. Recombinant human alpha 2-adrenoceptor subtypes: comparison of [3H]rauwolscine, [3H]atipamezole and [3H]RX821002 as radioligands. Biochim Biophys Acta 1995, 1266:207-214.
43. Harding C.F., Sheridan K., Walters M.J. Hormonal specificity and activation of sexual behavior in male zebra finches. Horm Behav 1983, 17:111-133.
44. Heimovics S.A., Cornil C.A., Ball G.F., Riters L.V. D1-like dopamine receptor density in nuclei involved in social behavior correlates with song in a context-dependent fashion in male European starlings. Neuroscience 2009, 159:962-973.
45. Heimovics S.A., Riters L.V. Immediate early gene activity in song control nuclei and brain areas regulating motivation relates positively to singing behavior during, but not outside of, a breeding context. J Neurobiol 2005, 65:207-224.
46. Heimovics S.A., Riters L.V. Breeding-context-dependent relationships between song and cFOS labeling within social behavior brain regions in male European starlings (Sturnus vulgaris). Horm Behav 2006, 50:726-735.
47. Heimovics S.A., Riters L.V. ZENK labeling within social behavior brain regions reveals breeding context-dependent patterns of neural activity associated with song in male European starlings (Sturnus vulgaris). Behav Brain Res 2007, 176:333-343.
48. Hull E.M., Dominguez J.M. Sexual behavior in male rodents. Horm Behav 2007, 52:45-55.
49. Kao M.H., Brainard M.S. Lesions of an avian basal ganglia circuit prevent context-dependent changes to song variability. J Neurophysiol 2006, 96:1441-1455.
50. Kao M.H., Wright B.D., Doupe A.J. Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context. J Neurosci 2008, 28:13232-13247.
51. Kelm C.A., Forbes-Lorman R.M., Auger C.J., Riters L.V. Mu-opioid receptor densities are depleted in regions implicated in agonistic and sexual behavior in male European starlings (Sturnus vulgaris) defending nest sites and courting females. Behav Brain Res 2010, 219:15-22.
52. Lehner P.N. Handbook of ethological methods 1996, Cambridge University Press, Cambridge.
53. Margoliash D. Functional organization of forebrain pathways for song production and perception. J Neurobiol 1997, 33:671-693.
54. Marler P.R., Slabbekoorn H. Nature's music: the science of birdsong 2004, Academic Press, San Diego, CA.
55. McGuire N.L., Bentley G.E. A functional neuropeptide system in vertebrate gonads: gonadotropin-inhibitory hormone and its receptor in testes of field-caught house sparrow (Passer domesticus). Gen Comp Endocrinol 2010, 166:565-572.
56. Meitzen J., Thompson C.K. Seasonal-like growth and regression of the avian song control system: neural and behavioral plasticity in adult male Gambel's white-crowned sparrows. Gen Comp Endocrinol 2008, 157:259-265.
57. Mello C.V., Pinaud R., Ribeiro S. Noradrenergic system of the zebra finch brain: immunocytochemical study of dopamine-beta-hydroxylase. J Comp Neurol 1998, 400:207-228.
58. Nordeen E.J., Nordeen K.W. Circuits and cellular mechanisms of sensory acquisition. Neuroscience of birdsong 2008, 256-270. Cambridge University Press, Cambridge. H.P. Ziegler, P.R. Marler (Eds.).
59. Nottebohm F. A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 1981, 214:1368-1370.
60. Nottebohm F., Kasparian S., Pandazis C. Brain space for a learned task. Brain Res 1981, 213:99-109.
61. O'Rourke M.F., Blaxall H.S., Iversen L.J., Bylund D.B. Characterization of [3H]RX821002 binding to alpha-2 adrenergic receptor subtypes. J Pharmacol Exp Ther 1994, 268:1362-1367.
62. Pryke S.R., Astheimer L.B., Buttemer W.A., Griffith S.C. Frequency-dependent physiological trade-offs between competing colour morphs. Biol Lett 2007, 3:494-497.
63. Riters L.V., Ball G.F. Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Horm Behav 1999, 36:276-286.
64. Riters L.V., Ball G.F. Sex differences in the densities of alpha 2-adrenergic receptors in the song control system, but not the medial preoptic nucleus in zebra finches. J Chem Neuroanat 2002, 23:269-277.
65. Riters L.V., Ball G.F. Sex differences in the densities of alpha(2)-adrenergic receptors in the song control system, but not the medial preoptic nucleus in zebra finches. J Chem Neuroanat 2002, 23:269-277.
66. Riters L.V., Eens M., Pinxten R., Ball G.F. Seasonal changes in the densities of alpha(2) noradrenergic receptors are inversely related to changes in testosterone and the volumes of song control nuclei in male European starlings. J Comp Neurol 2002, 444:63-74.
67. 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 2000, 38:250-261.
68. Riters L.V., Schroeder M.B., Auger C.J., Eens M., Pinxten R., Ball G.F. Evidence for opioid involvement in the regulation of song production in male European starlings. Behav Neurosci 2005, 119:245-255.
69. Riters L.V., Teague D.P., Schroeder M.B., Cummings S.E. Vocal production in different social contexts relates to variation in immediate early gene immunoreactivity within and outside of the song control system. Behav Brain Res 2004, 155:307-318.
70. Ruuskanen J.O., Laurila J., Xhaard H., Rantanen V.V., Vuoriluoto K., Wurster S., Marjamaki A., Vainio M., Johnson M.S., Scheinin M. Conserved structural, pharmacological and functional properties among the three human and five zebrafish alpha 2-adrenoceptors. Br J Pharmacol 2005, 144:165-177.
71. Shiflett M.W., Gould K.L., Smulders T.V., DeVoogd T.J. Septum volume and food-storing behavior are related in parids. J Neurobiol 2002, 51:215-222.
72. Sizemore M., Perkel D.J. Noradrenergic and GABA B receptor activation differentially modulate inputs to the premotor nucleus RA in zebra finches. J Neurophysiol 2008, 100:8-18.
73. 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 1997, 17:6001-6010.
74. Smith G.T., Brenowitz E.A., Wingfield J.C. Roles of photoperiod and testosterone in seasonal plasticity of the avian song control system. J Neurobiol 1997, 32:426-442.
75. Solis M.M., Perkel D.J. Noradrenergic modulation of activity in a vocal control nucleus in vitro. J Neurophysiol 2006, 95:2265-2276.
76. Starke K. Presynaptic autoreceptors in the third decade: focus on alpha2-adrenoceptors. J Neurochem 2001, 78:685-693.
77. Sughrue K.M., Brittingham M.C., French J.B.J. Endocrine effects of the herbicide linuron on the American goldfinch (Carduelis tristis). The Auk 2008, 125:411-419.
78. Taziaux M., Cornil C.A., Dejace C., Arckens L., Ball G.F., Balthazart J. Neuroanatomical specificity in the expression of the immediate early gene c-fos following expression of appetitive and consummatory male sexual behaviour in Japanese quail. Eur J Neurosci 2006, 23:1869-1887.
79. Theunissen F.E., Amin N., Shaevitz S., Woolley S.M.N., Fremouw T., Hauber M.E. Song selectivity and the songbird brain. Neuroscience of birdsong 2008, 157-173. Cambridge University Press, Cambridge. H.P. Ziegler, P.R. Marler (Eds.).
80. 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 2007, 104:15520-15525.
81. 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 2001, 122:1-9.
82. 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 2003, 57:130-140.
83. Van Hout A.J., Eens M., Balthazart J., Pinxten R. Complex modulation of singing behavior by testosterone in an open-ended learner, the European Starling. Horm Behav 2009, 56:564-573.
84. Wang Z., Young L.J., Liu Y., Insel T.R. Species differences in vasopressin receptor binding are evident early in development: comparative anatomic studies in prairie and montane voles. J Comp Neurol 1997, 378:535-546.
85. Wild M.J. Birdsong: anatomical foundations and central mechanisms of sensorimotor integration. Neuroscience of birdsong 2008, 136-152. Cambridge University Press, Cambridge. H.P. Ziegler, P.R. Marler (Eds.).
86. Williams T.D. Individual variation in endocrine systems: moving beyond the "tyranny of the Golden Mean". Philos Trans R Soc Lond B Biol Sci 2008, 363:1687-1698.
87. Wingfield J.C. Communicative behaviors, hormone-behavior interactions, and reproduction in vertebrates. Knobil and Neill's physiology of reproduction 2006, Vol. 1:1995-2030. Elsevier, St. Louis, San Diego, London. J.D. Neill (Ed.).
88. Wingfield J.C., Farner D.S. Endocrinology of reproduction in wild species. Avian biology 1993, Vol. 9:163-247. Academic Press, London. D.S. Farner (Ed.).