Plasticity in singing effort and its relationship with monoamine metabolism in the songbird telencephalon

Developmental Neurobiology

Volumn 70, Issue 1, 2010, Pages 41-57

  Salvante, Katrina G ^a   Racke, Danielle M ^a,b   Campbell, C Ryan ^a,c   Sockman, Keith W ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b WESTERN KENTUCKY UNIVERSITY   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

Bird song; Monoamines; Neuroplasticity; Norepinephrine; Serotonin

Indexed keywords

MONOAMINE; NORADRENALIN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COMPETITION; CONTROLLED STUDY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MALE; MATING; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN SECRETION; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; SINGING; SOCIAL ENVIRONMENT; SONGBIRD; STARLING; TELENCEPHALON;

ACOUSTIC STIMULATION; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMPETITIVE BEHAVIOR; DOPAMINE; ENVIRONMENT; MALE; NOREPINEPHRINE; SEROTONIN; SOCIAL BEHAVIOR; STARLINGS; TELENCEPHALON; TIME FACTORS; VOCALIZATION, ANIMAL;

EID: 73849084499     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20752     Document Type: Article

References (88)

1. Adret-Hausberger M, Jenkins PF. 1988. Complex organization of the warbling song in the European starling Sturnus vulgaris. Behaviour 107:138-156.
2. Appeltants D, Absil P, Balthazart J, Ball GF. 2000. Identification of the origin of catecholaminergic inputs to HVc in canaries by retrograde tract tracing combined with tyrosine hydroxylase immunocytochemistry. J Chem Neuroanat 18:117-133.
3. Appeltants D, Del Negro C, Balthazart J. 2002. Noradrenergic control of auditory information processing in female canaries. Behav Brain Res 133:221-235.
4. Azmitia EC, Segal M. 1978. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 179:641-668.
5. Ball GF, Auger CJ, Bernard DJ, Charlier TD, Sartor JJ, Riters LV, Balthazart J. 2004. Seasonal plasticity in the song control system: Multiple sites of steroid hormone action and the importance of variation in song behavior. Ann NY Acad Sci 1016:586-610.
6. Ball GF, Balthazart J. 2004. Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol Behav 83:329-346.
7. Ball GF, Castelino CB, Maney DL, Appeltants D, Balthazart J. 2003. The activation of birdsong by testosterone: Multiple sites of action and role of ascending catecholamine projections. Ann NY Acad Sci 1007:211-231.
8. Ball GF, Sockman KW, Duffy DL, Gentner TQ. 2006. A neuroethological approach to song behavior and perception in European starlings: Interrelationships among testosterone, neuroanatomy, immediate early gene expression, and immune function. Adv Stud Anim Behav 36:59-121.
9. Balthazart J. 1983. Hormonal correlates of behavior. In: Farner DS, King JR, Parkes KC, editors. Avian Biology, Vol 7. New York: Academic Press, pp 221-365.
10. Balthazart J, Ball GF. 2007. Topography in the preoptic region: Differential regulation of appetitive and consummatory male sexual behaviors. Front Neuroendocrin 28:161-178.
11. Barclay SR, Harding CF. 1988. 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 459:333-343.
12. Barclay SR, Harding CF. 1990. 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 523:251-262.
13. Barclay SR, Harding CF, Waterman SA. 1991. Correlations between catecholamine levels and sexual behavior in male zebra finches. Pharmacol Biochem Behav 41:195-201.
14. Barclay SR, Harding CF, Waterman SA. 1996. Central DSP-4 treatment decreases norepinephrine levels and courtship behavior in male zebra finches. Pharmacol Biochem Behav 53:213-220.
15. Bauer EE, Coleman MJ, Roberts TF, Roy A, Prather JF, Mooney R. 2008. A synaptic basis for auditory-vocal integration in the songbird. J Neurosci 28:1509-1522.
16. Bell AM, Backstrom T, Huntingford FA, Pottinger TG, Winberg S. 2007. Variable neuroendocrine responses to ecologically-relevant challenges in sticklebacks. Physiol Behav 91:15-25.
17. Berridge C, Waterhouse B. 2003. The locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev 42:33-84.
18. Bobillier P, Seguin S, Petitjean F, Salvert D, Touret M, Jouvet M. 1976. The raphe nuclei of the cat brain stem: A topographical atlas of their efferent projections as revealed by autoradiography. Brain Res 113:449-486.
19. Bradford MM. 1976. A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248-254.
20. Brainard MS. 2004. Contributions of the anterior forebrain pathway to vocal plasticity. Ann NY Acad Sci 1016:377-394.
21. Burnham HP, Anderson DR. 2003. Model Selection and Multi-Model Inference. Berlin: Springer, 496 p.
22. Burton P, Gurrin L, Sly P. 1998. Extending the simple linear regression model to account for correlated responses: An introduction to generalized estimating equations and multi-level mixed modelling. Stat Med 17:1261-1291.
23. Castelino CB, Ball GF. 2005. A role for norepinephrine in the regulation of context-dependent ZENK expression in male zebra finches (Taeniopygia guttata). Eur J Neurosci 21:1962-1972.
24. Catchpole CK, Slater PJB. 1995. Bird Song. Cambridge: Cambridge University Press, 256 p.
25. Dave AS, Yu AC, Margoliash D. 1998. Behavioral state modulation of auditory activity in a vocal motor system. Science 282:2250-2254.
26. Doupe AJ, Konishi M. 1991. Song-selectig auditory circuits in the vocal control system of the zebra finch. Proc Natl Acad Sci USA 88:11339-11343.
27. Doupe AJ, Perkel DJ, Reiner A, Stern EA. 2005. Birdbrains could teach basal ganglia research a new song. Trends Neurosci 28:353-363.
28. Duffy DL, Ball GF. 2002. Song predicts immunocompetence in male European starlings (Sturnus vulgaris). Proc R Soc Lond B 269:847-852.
29. Eens M. 1997. Understanding the complex song of the European starling: An integrated ethological approach. Adv Stud Behav 26:355-434.
30. Eens M, Pinxten R, Verheyen RF. 1989. Temporal and sequential organization of song bouts in the starling. Ardea 77:75-85.
31. Eens M, Pinxten R, Verheyen RF. 1991. Male song as a cue for mate choice in the European starling. Behaviour 116:210-238.
32. Feare CJ. 1984. The Starling. Oxford: Oxford University Press, 328 p.
33. Gahr M. 2004. Hormone-dependent neural plasticity in the juvenile and adult song system. Ann NY Acad Sci 1016:684-703.
34. Gentner TQ, Hulse SH. 2000. Female European starling preference and choice for variation in conspecific male song. Anim Behav 59:443-458.
35. Gentner TQ, Hulse SH, Duffy D, Ball GF. 2001. Response biases in aditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J Neurobiol 46:48-58.
36. Gil D, Gahr M. 2002. The honesty of bird song: Multiple constraints for multiple traits. Trends Ecol Evol 17:133-141.
37. Goldstein H, Brown W, Rasbash J. 2002. Multilevel modeling of medical data. Stat Med 21:3291-3315.
38. Halaris AE, Jones BE, Moore RY. 1976. Axonal transport in serotonin neurons of the midbrain raphe. Brain Res 107:555-574.
39. Harding CF. 2004. Hormonal modulation of singing: Hormonal modulation of the songbird brain and singing behavior. Ann NY Acad Sci 1016:524-539.
40. Harding CF, Sheridan K, Walters MJ. 1983. Hormonal specificity and activation of sexual behavior in male zebra finches. Horm Behav 17:111-133.
41. Heimovics SA, Cornil CA, Ball GF, Riters LV. 2009. D1-like dopamine receptor density in nuclei involved in social behavior correlates with song in a context-dependent fashion in male European starlings. Neuroscience 159:962-973.
42. Heimovics SA, Riters LV. 2005. 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 65:207-224.
43. Heimovics SA, Riters LV. 2006. Breeding-context dependent relationships between song and cFOS labeling within social behavior brain regions in male European starlings (Sturnus vulgaris). Horm Behav 50:726-735.
44. Heimovics SA, Riters LV. 2007. ZENK labeling within social behavior brain regions reveals breeding contextdependent patterns of neural activity associated with song in male European starlings (Sturnus vulgaris). Behav Brain Res 176:333-343.
45. Hessler NA, Doupe AJ. 1999. Social context modulates singing-related neural activity in the songbird forebrain. Nature Neurosci 2:209-211.
46. Hull EM, Lorrain DS, Du J, Matuszewich L, Lumley LA, Putnam SK, Moses J. 1999. Hormone-meurotransmitter interactions in the control of sexual behavior. Behav Brain Res 105:105-116.
47. Hurley LM, Devilbiss DM, Waterhouse BD. 2004. A matter of focus: Monoaminergic modulation of stimulus coding in mammalian sensory networks. Curr Opin Neurobiol 14:488-495.
48. Hurley LM, Pollak G. 1999. Serotonin differentially modulates responses to tones and frequency-modulated sweeps in the inferior colliculus. J Neurosci 19:8071-8082.
49. Hurley LM, Pollak G. 2001. Serotonin effects on frequency tuning of inferior colliculus neurons. J Neurophysiol 85:828-842.
50. Hurley LM, Pollak G. 2005. Serotonin modulates responses to species-specific vocalizations in the interior colliculus. J Comp Physiol A 191:535-546.
51. Hurley LM, Thompson AM, Pollak GD. 2002. Serotonin in the inferior colliculus. Hear Res 168:1-11.
52. Jacobs BJ, Azmitia EC. 1992. Structure and function of the brain-serotonin system. Physiol Rev 72:165-229.
53. Jarvis ED, Nottebohm F. 1997. Moter-driven gene expression. Proc Natl Acad Sci USA 94:4097-4102.
54. Jarvis ED, Scharff C, Grossman MR, Ramos JA, Nottebohm F. 1998. For whom the birds sings: Context-dependent gene expression. Neuron 21:775-788.
55. Kessel B. 1951. Criteria for sexing and aging European starlings (Sturnus vulgaris). Bird Banding 22:16-23.
56. Kilts CD, Breese GR, Mailman RB. 1981. Simultaneous quantification of dopamine, 5-hydroxytryptamine and four metabolically related compounds by means of reversed-phase high-performance liquid chromatography with electrochemical detection. J Chromatogr-Biomed 225:347-357.
57. Klepper A, Herbert H. 1991. Distribution and origin of noradrenergic and serotonergic fibers in the cochlear nucleus and inferior colliculous of the rat. Brain Res 557:180-201.
58. Kroodsma DE, Byers BE, Goodale E, Johnson S, Liu W-C. 2001. Pseudoreplication in playback experiments, revisited a decade later. Anim Behav 61:1029-1033.
59. MacDougall-Shackleton SA, Hulse SH, Ball GF. 1998. Neural bases of song preferences in female zebra finches (Taeniopygia guttata). Neuro Report 9:3047-3052.
60. Maney DL, Ball GF. 2003. Fos-like immunoreactivity in catecholaminergic brain nuclei after territorial behavior in free-living song sparrows. J Neurobiol 56:163-170.
61. Meitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ. 2007. Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 27:12045-12057.
62. Mello CV, Pinaud R, Ribeiro S. 1998. Noradrenergic system of the zebra finch brain: Immunocytochemical study of dopamine-β-hydroxylase. J Comp Neurol 400:207-228.
63. Mello CV, Ribeiro S. 1998. ZENK protein regulation by song in the brain of songbirds. J Comp Neurol 393:426-438.
64. Mello CV, Vicario DS, Clayton DF. 1992. Song presentation induces gene expression in the songbird forebrain. Proc Natl Acan Sci USA 89:6818-6822.
65. Moore KE. 1986. Drug-induced changes in the efflux of dopamine and serotonin metabolites from the brains of freely moving rats. Ann NY Acad Sci 473:303-320.
66. Moore RY, Halaris AE, Jones BE. 1978. Serotonin neurons of the midbrain raphe: Ascending projections. J Comp Neurol 180:416-438.
67. Mountjoy DJ, Lemon RE. 1991. Song as an attractant for male and female European starlings, and the influence of song complexity on their response. Behav Ecol Sociobiol 28:97-100.
68. Mountjoy DJ, Lemon RE. 1996. Female choice for complex song in the European starling: A field experiment. Behav Ecol Sociobiol 38:65-71.
69. Nicholls TJ, Goldsmith AR, Dawson A. 1988. Photorefractoriness in birds and comparison with mammals. Physiol Rev 68:133-176.
70. Nottebohm F, Stokes TM, Leonard CM. 1976. Central control of song in the canary, Serinus canaria. J Comp Neurol 165:457-486.
71. Rabe-Hesketh S, Skrondal A. 2005. Multilevel and Longitudinal Modeling Using Stata. College Station, TX: Stata Press,320 p.
72. Remage-Healey L, Maidment NT, Schlinger BA. 2008. Forebrain steroid levels fluctuate rapidly during social interactions. Nat Neurosci 11:1327-1334.
73. Riters LV, Ball GF. 1999. Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Horm Behav 36:276-286.
74. Riters LV, Eens M, Pinxten R, Duffy DL, Balthazart J, Ball GF. 2000. Seasonal changes in courtship song and the medial preoptic area in male Europoean starlings (Sturnus vulgaris). Horm Behav 38:250-261.
75. Riters LV, Teague DP, Schroeder MB, Cummings SE. 2004. 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 155:307-318.
76. Sasaki A, Sotnikova TD, Gainetdinov RR, Jarvis ED. 2006. Social context-dependent singing-regulated dopamine. J Neurosci 26:9010-9014.
77. Schlinger BA. 1997. Sex steroids and their actions on the birdsong system. J Neurobiol 33:619-631.
78. Sewards TV, Sewards MA. 2003. Representations of motivational drives in mesial cortex, medial thalamus, hypothalamus and midbrain. Brain Res Bull 61:25-49.
79. Sockman KW. 2007. Neural orchestration of mate-choice plasticity in songbirds. J Ornith 148:S225-S230.
80. Sockman KW, Gentner TQ, Ball GF. 2002. Recent experience modulates forebrain gene-expression in response to mate-choice cues in European starlings. Proc Roy Soc Lond B 269:2479-2485.
81. Sockman KW, Gentner TQ, Ball GF. 2005a. Complimentary neural systems for the experience-dependent integration of mate-choice cues in European starlings. J Neurobiol 62:72-81.
82. Sockman KW, Salvante KG. 2008. The integration of song environment by catecholaminergic systems innervating the auditory telencephalon of adult female European starlings. Develop Neurobiol 68:656-668.
83. Sockman KW, Salvante KG, Racke DM, Campbell CR, Whitman BA. 2009. Song compeition changes the brain and behavior of amale songbird. J Exp Biol 212:2411-2418.
84. Sockman KW, Sewall KB, Ball GF, Hahn TP. 2005b. Economy of mate attraction in the Cassin's finch. Biol Lett-UK 1:34-37.
85. Sockman KW, Weiss J, Webster MS, Talbott V, Schwabl H. 2008. Sex-specific effects of yolk-androgens on growth of American kestrels. Behav Ecol Sociobiol 62:617-625.
86. Vates GE, Broome BM, Mello CV, Nottebohm F. 1996. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata). J Comp Neurol 366:613-642.
87. Wiley RH. 2003. Is there an ideal behavioural experiment? Anim Behav 66:585-588.
88. Wingfield JC, Farner DS. 1993. Endocrinology of reproduction in wild species. In: Farner DS, King JR, Parkes KC, editors. Avian Biology, Vol 9. New York: Academic Press, pp 163-327.