Rapid effects of hearing song on catecholaminergic activity in the songbird auditory pathway

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Matragrano, Lisa L ^a   Beaulieu, Michaël ^b   Phillip, Jessica O ^a   Rae, Ali I ^a   Sanford, Sara E ^a   Sockman, Keith W ^b,c   Maney, Donna L ^a  

^a EMORY UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXY 3 METHOXYPHENYLETHYLENE GLYCOL; CATECHOLAMINE; DIHYDROXYPHENYLACETIC ACID; ESTROGEN; HOMOVANILLIC ACID; NORADRENALIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; AUDITORY SYSTEM; CATECHOLAMINE SYNTHESIS; CATECHOLAMINERGIC SYSTEM; ENZYME PHOSPHORYLATION; EXPOSURE; FEMALE; FOREBRAIN; HEARING; HEMISPHERIC DOMINANCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MESENCEPHALON; METABOLITE; NONHUMAN; SONGBIRD; THALAMUS; VOCALIZATION;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PATHWAYS; CATECHOLAMINES; FEMALE; HEARING; MALE; NEURONS; PHOSPHORYLATION; SINGING; SONGBIRDS; TYROSINE 3-MONOOXYGENASE; VOCALIZATION, ANIMAL;

EID: 84862576551     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039388     Document Type: Article

References (99)

1. Aston-Jones G, Cohen JD, (2005) An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annu Rev Neurosci 28: 403-450.
2. 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.
3. Bao S, Chan VT, Merzenich MM, (2001) Cortical remodeling induced by activity of ventral tegmental dopamine neurons. Nature 412: 79-83.
4. Berridge CW, Waterhouse BD, (2003) The locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev 42: 33-84.
5. Appeltants D, Ball GF, Balthazart J, (2001) The distribution of tyrosine hydroxylase in the canary brain: Demonstration of a specific and sexually dimorphic catecholaminergic innervation of the telencephalic song control nuclei. Cell Tissue Res 304: 237-259.
6. Appeltants D, Del Negro C, Balthazart J, (2002) Noradrenergic control of auditory information processing in female canaries. Behav Brain Res 133: 221-235.
7. Appeltants D, Gentner TQ, Hulse SH, Balthazart J, Ball GF, (2005) The effect of auditory distractors on song discrimination in male canaries. Behav Processes 69: 331-341.
8. Bharati IS, Goodson JL, (2006) Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches. Neuroscience 143: 661-670.
9. Cardin JA, Schmidt MF, (2004) Noradrenergic inputs mediate state dependence of auditory responses in the avian song system. J Neurosci 24: 7745-7753.
10. LeBlanc MM, Goode CT, MacDougall-Shackleton EA, Maney DL, (2007) Estradiol modulates brainstem catecholaminergic cell groups and projections to the auditory forebrain in a female songbird. Brain Res 1171: 93-103.
11. 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.
12. Riters LV, Pawlisch BA, (2007) Evidence that norepinephrine influences responses to male courtship song and activity within song control regions and the ventromedial nucleus of the hypothalamus in female European starlings. Brain Res 1149: 127-140.
13. Castelino CB, Schmidt MF, (2010) What birdsong can teach us about the central noradrenergic system. J Chem Neuroanat 39: 96-111.
14. Appeltants D, Ball GF, Balthazart J, (2002) The origin of catecholaminergic inputs to the song control nucleus RA in canaries. Neuroreport 13: 649-653.
15. Lynch KS, Ball GF, (2008) Noradrenergic deficits alter processing of communication signals in female songbirds. Brain Behav Evol 72: 207-214.
16. Vyas A, Harding C, McGowan J, Snare R, Bogdan D, (2008) Noradrenergic neurotoxin, N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine hydrochloride (DSP-4), treatment eliminates estrogenic effects on song responsiveness in female zebra finches (Taeniopygia guttata). Behav Neurosci 122: 1148-1157.
17. Pawlisch BA, Riters LV, (2010) Selective behavioral responses to male song are affected by the dopamine agonist GBR-12909 in female European starlings (Sturnus vulgaris). Brain Res 1353: 113-124.
18. Pawlisch BA, Stevenson SA, Riters LV, (2011) Alpha-1-Noradrenegic receptor antagonism disrupts female songbird responses to male song. Neurosci Lett 496: 20-24.
19. Matragrano LL, Sanford SE, Salvante KG, Sockman KW, Maney DL, (2011) Estradiol-dependent catecholaminergic innervation of auditory areas in a seasonally breeding songbird. Eur J Neurosci 34: 416-425.
20. Sockman KW, Salvante KG, (2008) The integration of song environment by catecholaminergic systems innervating the auditory telencephalon of adult female European starlings. Dev Neurobiol 68: 656-668.
21. Grace AA, (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: A hypothesis for the etiology of schizophrenia. Neuroscience 41: 1-24.
22. Beaudet A, Descarries L, (1978) The monoamine innervation of rat cerebral cortex: synaptic and nonsynaptic axon terminals. Neuroscience 3: 851-860.
23. Reader TA, Ferron A, Descarries L, Jasper HH, (1979) Modulatory role for biogenic amines in the cerebral cortex. Microiontophoretic studies. Brain Res 160: 217-229.
24. Schultz W, (2007) Multiple dopamine functions at different time courses. Annu Rev Neurosci 30: 259-288.
25. Valentino RJ, van Bockstaele E, (2008) Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur J Pharmacol 583: 194-203.
26. Clayton DF, (2000) The genomic action potential. Neurobiol Learn Mem 74: 185-216.
27. Nordeen EJ, Holtzman DA, Nordeen KW, (2009) Increased fos expression among midbrain dopaminergic cell groups during birdsong tutoring. Eur J Neurosci 30: 662-670.
28. Maney DL, Goode CT, Lange HS, Sanford SE, Solomon BL, (2008) Estradiol modulates neural responses to song in a seasonal songbird. J Comp Neurol 511: 173-186.
29. Gale SD, Perkel DJ, (2010) A basal ganglia pathway drives selective auditory responses in songbird dopaminergic neurons via disinhibition. J Neurosci 30: 1027-1037.
30. Doupe AJ, (1997) Song- and order-selective neurons in the songbird anterior forebrain and their emergence during vocal development. J Neurosci 17: 1147-1167.
31. Margoliash D, (1997) Functional organization of forebrain pathways for song production and perception. J Neurobiol 33: 671-693.
32. Xu ZQ, Lew JY, Harada K, Aman K, Goldstein M, et al. (1998) Immunohistochemistry studies on phosphorylation of tyrosine hydroxylase in central catecholamine neurons using site- and phosphorylation state-specific antibodies. Neuroscience 82: 727-738.
33. Fujisawa H, Okunu S, (2005) Regulatory mechanism of tyrosine hydroxylase activity. Biochem Biophys Res Commun 338: 271-276.
34. Kumer SC, Vrana KE, (1996) Intricate regulation of tyrosine hydroxylase activity and gene expression. J Neurochem 67: 443-462.
35. Salvatore MF, Garcia-Espana A, Goldstein M, Deutch AY, Haycock JW, (2000) Stoichiometry of tyrosine hydroxylase phosphorylation in the nigrostriatal and mesolimbic systems in vivo: effects of acute haloperidol and related compounds. J Neurochem 75: 225-232.
36. Dunkley PR, Bobrovskaya L, Graham ME, von Nagy-Felsobuki EI, Dickson PW, (2004) Tyrosine hydroxylase phosphorylation: regulation and consequences. J Neurochem 91: 1025-1043.
37. Gammie SC, Edelmann MN, Mandel-Brehm C, D'Anna KL, Auger AP, et al. (2008) Altered dopamine signaling in naturally occurring maternal neglect. PLoS ONE 3: e1974.
38. Riters LV, Olesen KM, Auger CJ, (2007) Evidence that female endocrine state influences catecholamine responses to male courtship song in European starlings. Gen Comp Endocrinol 154: 137-149.
39. Maney DL, Pinaud R, (2011) Estradiol-dependent modulation of auditory processing and selectivity in songbirds. Front Neuroendocrinol 32: 287-302.
40. Karten HJ, (1967) The organization of the ascending auditory pathway in the pigeon (Columba livia). I. Diencephalic projections of the inferior colliculus (nucleus mesencephalicus lateralis, pars dorsalis). Brain Res 6: 409-427.
41. Amin N, Gill P, Theunissen FE, (2010) Role of the zebra finch auditory thalamus in generating complex representations for natural sounds. J Neurophysiol 104: 784-798.
42. Woolley SM, Fremouw TE, Hsu A, Theunissen FE, (2005) Tuning for spectro-temporal modulations as a mechanism for auditory discrimination of natural sounds. Nat Neurosci 8: 1371-1379.
43. 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 (Taeniopygia guttata). J Comp Neurol 366: 613-642.
44. Pinaud R, Terleph TA, (2008) A songbird forebrain area potentially involved in auditory discrimination and memory formation. J Biosci 33: 145-155.
45. Tremere LA, Jeong JK, Pinaud R, (2009) Estradiol shapes auditory processing in the adult brain by regulating inhibitory transmission and plasticity-associated gene expression. J Neurosci 29: 5949-5963.
46. Matragrano LL, Sanford SE, Salvante KG, Beaulieu M, Sockman KW, et al. (2012) Estradiol-dependent modulation of serotonergic markers in auditory areas of a seasonally breeding songbird. Behav Neurosci 126: 110-122.
47. Avey MT, Phillmore LS, MacDougall-Shackleton SA, (2005) Immediate early gene expression following exposure to acoustic and visual components of courtship in zebra finches. Behav Brain Res 165: 247-253.
48. George I, Vernier B, Richard JP, Hausberger M, Cousillas H, (2004) Hemispheric specialization in the primary auditory area of awake and anesthetized starlings (Sturnus vulgaris). Behav Neurosci 118: 597-610.
49. Phan ML, Vicario DS, (2010) Hemispheric differences in processing of vocalizations depend on early experience. Proc Natl Acad Sci U S A 107: 2301-2306.
50. Poirier C, Boumans T, Verhoye M, Balthazart J, Van der Linden A, (2009) Own-song recognition in the songbird auditory pathway: selectivity and lateralization. J Neurosci 29: 2252-2258.
51. Goodson JL, Kabelik D, Kelly AM, Rinaldi J, Klatt JD, (2009) Midbrain dopamine neurons reflect affiliation phenotypes in finches and are tightly coupled to courtship. Proc Natl Acad Sci U S A 106: 8737-8742.
52. Daubner SC, Le T, Wang S, (2011) Tyrosine hydroxylase and regulation of dopamine synthesis. Arch Biochem Biophys 508: 1-12.
53. Robinson PJ, Dunkley PR, (1985) Depolarisation-dependent protein phosphorylation and dephosphorylation in rat cortical synaptosomes is modulated by calcium. J Neurochem 44: 338-348.
54. Ong LK, Guan L, Stutz B, Dickson PW, Dunkley PR, et al. (2011) The effects of footshock and immobilization stress on tyrosine hydroxylase phosphorylation in the rat locus coeruleus and adrenal gland. Neuroscience 192: 20-27.
55. Niu X, Canlon B, (2002) Activation of tyrosine hydroxylase in the lateral efferent terminals by sound conditioning. Hear Res 174: 124-132.
56. Cransac H, Cottet-Emard JM, Hellström S, Peyrin L, (1998) Specific sound-induced noradrenergic and serotonergic activation in central auditory structures. Hear Res 118: 151-156.
57. Ong LK, Bobrovskaya L, Walker FR, Day TA, Dickson PW, et al. (2011) The effect of social defeat on tyrosine hydroxylase phosphorylation in the rat brain and adrenal gland. Neurochem Res 36: 27-36.
58. Brown EE, Damsma G, Cumming P, Fibiger HC, (1991) Interstitial 3-methoxytyramine reflects striatal dopamine release: an in vivo microdialysis study. J Neurochem 57: 701-707.
59. Commissiong JW (1985) Monoamine metabolites: Their relationship and lack of relationship to monoaminergic neuronal activity. Biochem Pharmacol 34: 1127-1131.
60. 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.
61. Stark H, Scheich H, (1997) Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: A long-term microdialysis study of metabolites. J Neurochem 68: 691-697.
62. Soares-da-Silva P, (1987) Does brain 3,4-dihydroxyphenylacetic acid reflect dopamine release? J Pharm Pharmacol 39: 127-129.
63. Soares-da-Silva P, Garrett MC, (1990) A kinetic study of the rate of formation of dopamine, 3,4-dihydroxyphenylacetic acid (DOPAC) and homovanillic acid (HVA) in the brain of the rat: implications for the origin of DOPAC. Neuropharmacology 29: 869-874.
64. Zetterstrom T, Sharp T, Collin AK, Ungerstedt U, (1988) In vivo measurement of extracellular dopamine and DOPAC in rat striatum after various dopamine-releasing drugs; implications for the origin of extracellular DOPAC. Eur J Pharmacol 148: 327-334.
65. Abercrombie ED, Keefe KA, DiFrischia DS, Zigmond MJ, (1989) Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 52: 1655-1658.
66. Gresch PJ, Sved AF, Zigmond MJ, Finlay JM, (1994) Stress-induced sensitization of dopamine and norepinephrine efflux in medial prefrontal cortex of the rat. J Neurochem 63: 575-583.
67. Curtis AL, Leiser SC, Snyder K, Valentino RJ, (2012) Predator stress engages corticotropin-releasing factor and opioid systems to alter the operating mode of locus coeruleus norepinephrine neurons. Neuropharmacology 62: 1737-1745.
68. Leviel V, (2001) The reverse transport of DA, what physiological significance? Neurochem Int 38: 83-106.
69. Hurley LM, Hall IC, (2011) Context-dependent modulation of auditory processing by serotonin. Hear Res 279: 74-84.
70. Sockman KW, Gentner TQ, Ball GF, (2002) Recent experience modulates forebrain gene-expression in response to mate-choice cues in European starlings. Proc R Soc Lond 269: 2479-2485.
71. Maney DL, Cho E, Goode CT, (2006) Estrogen dependent selectivity of genomic responses to birdsong. Eur J Neurosci 23: 1523-1529.
72. Sanford SE, Lange HS, Maney DL, (2010) Topography of estradiol-modulated genomic responses in the songbird auditory forebrain. Dev Neurobiol 70: 73-86.
73. Miranda JA, Liu RC, (2009) Dissecting natural sensory plasticity: Hormones and experience in a maternal context. Hear Res 252: 21-28.
74. Griffiths R, Double MC, Orr K, Dawson RJ, (1998) A DNA test to sex most birds. Mol Ecol 7: 1071-1075.
75. Wolfson A, (1958) Regulation of refractory period in the photoperiodic responses of the white-throated sparrow. J Exp Zool 139: 349-379.
76. Shank MC, (1959) The natural termination of the refractory period in the slate-colored junco and in the white-throated sparrow. Auk 76: 44-54.
77. Lake JI, Lange HS, O'Brien S, Sanford SE, Maney DL, (2008) Activity of the hypothalamic-pituitary-gonadal axis differs between behavioral phenotypes in female white-throated sparrows (Zonotrichia albicollis). Gen Comp Endocrinol 156: 426-433.
78. Maney DL, Goode CT, Lake JI, Lange HL, O'Brien S, (2007) Rapid neuroendocrine responses to auditory courtship signals. Endocrinology 148: 5614-5623.
79. Moore MC, (1983) Effect of female sexual displays on the endocrine physiology and behavior of male white-crowned sparrows, Zonotrichia leucophrys. J Zool 199: 137-148.
80. Maney DL, MacDougall-Shackleton EA, MacDougall-Shackleton SA, Ball GF, Hahn TP, (2003) Immediate early gene response to hearing correlates with receptive behavior and depends on dialect in a female bird. J Comp Physiol A 189: 667-674.
81. Maney DL, Lange HS, Raees MQ, Reid AE, Sanford SE, (2009) Behavioral phenotypes persist after gonadal steroid manipulation in white-throated sparrows. Horm Behav 55: 113-120.
82. Falls JB, Kopachena JG, (1994) White-throated sparrow (Zonotrichia albicollis). In: Poole A, Gill F, editors. editors. The Birds of North America, No. 128, Philadelphia: The Academy of Natural Sciences and Washington, D.C.: The American Ornithologists' Union, 1-30.
83. Maney DL, Erwin KL, Goode CT, (2005) Neuroendocrine correlates of behavioral polymorphism in white-throated sparrows. Horm Behav 48: 196-206.
84. Shu SY, Ju G, Fan LZ, (1988) The glucose-oxidase DAB nickel method in peroxidase histochemistry of the nervous system. Neurosci Lett 85: 169-171.
85. Maney DL, Bernard DJ, Ball GF, (2001) Gonadal steroid receptor mRNA in catecholaminergic nuclei of the canary brainstem. Neurosci Lett 311: 189-192.
86. Reiner A, Karle EJ, Anderson KD, Medina L, (1994) Catecholaminergic perikarya and fibers in the avian nervous system. In: Smeets WFA, Reiner A, editors. editors. Phylogeny and development of catecholamine system in the CNS of vertebrates. Cambridge: Cambridge University Press, 135-181.
87. Saper CB, Sawchenko PE, (2003) Magic peptides, magic antibodies: Guidelines for appropriate controls for immunohistochemistry. J Comp Neurol 465: 161-163.
88. Olsson C, Holmberg A, Holmgren S, (2008) Development of enteric and vagal innervation of the zebrafish (Danio rerio) gut. J Comp Neurol 508: 756-770.
89. Bailhache T, Balthazart J, (1993) The catecholaminergic system of the quail brain- immunocytochemical studies of dopamine beta-hydroxylase and tyrosine-hydroxylase. J Comp Neurol 329: 230-256.
90. Moons L, van Gills J, Ghijsels E, Vandensande F, (1994) Immunocytochemical localization of the L-DOPA and dopamine in the brain of the chicken (Gallus domesticus). J Comp Neurol 346: 97-118.
91. Soha JA, Shimizu T, Doupe AJ, (1996) Development of the catecholaminergic innervation of the song system of the male zebra finch. J Neurobiol 29: 473-489.
92. Roberts TF, Cookson KK, Heaton KJ, Hall WS, Brauth SE, (2001) Distribution of tyrosine hydroxylase-containing neurons and fibers in the brain of the budgerigar (Melopsittacus undulatus): General patterns and labeling in vocal control nuclei. J Comp Neurol 429: 436-454.
93. Balthazart J, Ball GF, (1996) Identification of catecholaminergic cell groups in the brainstem of the canary, zebra finch, white-throated sparrow and budgerigar by tyrosine-hydroxylase immunohistochemistry. Belg J Zool 126: 65-78.
94. Bottjer SW, (1993) The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. J Neurobiol 24: 51-69.
95. Metzger M, Jiang S, Wang J, Braun K, (1996) Organization of the dopaminergic innervation of forebrain areas relevant to learning: A combined immunohistochemical/retrograde tracing study in the domestic chick. J Comp Neurol 376: 1-27.
96. Zeng S, Li J, Zhang X, Zuo M, (2007) Distinction of neurochemistry between the cores and their shells of auditory nuclei in tetrapod species. Brain Behav Evol 70: 1-20.
97. Logerot P, Krutzfeldt NOE, Wild JM, Kubke MF, (2011) Subdivisions of the auditory midbrain (n. mesencephalicus lateralis, pars dorsalis) in zebra finches using calcium-binding protein immunocytochemistry. PLoS ONE 6: e20686.
98. 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 225: 347-357.
99. 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.