Noradrenergic control of gene expression and long-term neuronal adaptation evoked by learned vocalizations in songbirds

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Velho, Tarciso A F ^a,d   Lu, Kai ^b   Ribeiro, Sidarta ^c   Pinaud, Raphael ^a,e   Vicario, David ^b   Mello, Claudio V ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ADRENERGIC RECEPTOR; NORADRENALIN; ALPHA 1 ADRENERGIC RECEPTOR; ALPHA ADRENERGIC RECEPTOR BLOCKING AGENT; IMMEDIATE EARLY PROTEIN;

ADAPTATION; ANIMAL BEHAVIOR; ARTICLE; AUDITORY MEMORY; AUDITORY NERVOUS SYSTEM; AUDITORY RESPONSE; CONTROLLED STUDY; DENSITOMETRY; ELECTROPHYSIOLOGY; FEMALE; GENE EXPRESSION; GENETIC ANALYSIS; NERVE STIMULATION; NONHUMAN; NORADRENERGIC SYSTEM; SONGBIRD; SPEECH; VOCALIZATION; ZEBRA FISH; ADRENERGIC NERVE CELL; ANIMAL; AUDITORY STIMULATION; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; LEARNING; MEMORY; METABOLISM; PHYSIOLOGY; TELENCEPHALON; TIME;

TAENIOPYGIA GUTTATA;

ACOUSTIC STIMULATION; ADAPTATION, PHYSIOLOGICAL; ADRENERGIC ALPHA-ANTAGONISTS; ADRENERGIC NEURONS; ANIMALS; FEMALE; GENE EXPRESSION REGULATION; IMMEDIATE-EARLY PROTEINS; LEARNING; MEMORY; PASSERIFORMES; RECEPTORS, ADRENERGIC, ALPHA-1; TELENCEPHALON; TIME FACTORS; VOCALIZATION, ANIMAL;

EID: 84860517181     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036276     Document Type: Article

References (55)

1. Aston-Jones G, Bloom FE, (1981) Nonrepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J Neurosci 1: 887-900.
2. Foote SL, Aston-Jones G, Bloom FE, (1980) Impulse activity of locus coeruleus neurons in awake rats and monkeys is a function of sensory stimulation and arousal. Proc Natl Acad Sci U S A 77: 3033-3037.
3. Murchison CF, Zhang XY, Zhang WP, Ouyang M, Lee A, et al. (2004) A distinct role for norepinephrine in memory retrieval. Cell 117: 131-143.
4. McGaugh JL, (2000) Memory-a century of consolidation. Science 287: 248-251.
5. 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.
6. Ramos BP, Arnsten AF, (2007) Adrenergic pharmacology and cognition: focus on the prefrontal cortex. Pharmacol Ther 113: 523-536.
7. McGaugh JL, Izquierdo I, (2000) The contribution of pharmacology to research on the mechanisms of memory formation. Trends Pharmacol Sci 21: 208-210.
8. Cirelli C, Pompeiano M, Tononi G, (1996) Neuronal gene expression in the waking state: a role for the locus coeruleus. Science 274: 1211-1215.
9. Cirelli C, Tononi G, (2000) Differential expression of plasticity-related genes in waking and sleep and their regulation by the noradrenergic system. Journal of Neuroscience 20: 9187-9194.
10. Walling SG, Harley CW, (2004) Locus ceruleus activation initiates delayed synaptic potentiation of perforant path input to the dentate gyrus in awake rats: a novel beta-adrenergic- and protein synthesis-dependent mammalian plasticity mechanism. J Neurosci 24: 598-604.
11. Stanton PK, Sarvey JM, (1985) Depletion of norepinephrine, but not serotonin, reduces long-term potentiation in the dentate gyrus of rat hippocampal slices. J Neurosci 5: 2169-2176.
12. Brenowitz EA, Margoliash D, Nordeen KW, (1997) An introduction to birdsong and the avian song system. Journal of Neurobiology 33: 495-500.
13. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, et al. (2000) Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20: 3993-4001.
14. Jones MW, Errington ML, French PJ, Fine A, Bliss TV, et al. (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4: 289-296.
15. Mello CV, Vicario DS, Clayton DF, (1992) Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci U S A 89: 6818-6822.
16. Velho TA, Pinaud R, Rodrigues PV, Mello CV, (2005) Co-induction of activity-dependent genes in songbirds. Eur J Neurosci 22: 1667-1678.
17. Wang Y, Brzozowska-Prechtl A, Karten HJ, (2010) Laminar and columnar auditory cortex in avian brain. Proc Natl Acad Sci U S A 107: 12676-12681.
18. Gobes SM, Bolhuis JJ, (2007) Birdsong memory: a neural dissociation between song recognition and production. Curr Biol 17: 789-793.
19. Velho TAF, Mello CV, (2007) Transcriptional regulation of activity-dependent genes by birdsong. In: Dudek S, editors. Transcriptional Regulation by Neuronal Activity 1st ed Springer pp. 3-26.
20. Chew SJ, Mello C, Nottebohm F, Jarvis E, Vicario DS, (1995) Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain. Proc Natl Acad Sci U S A 92: 3406-3410.
21. Clayton DF, (2000) The genomic action potential. Neurobiol Learn Mem 74: 185-216.
22. Mello CV, Velho TA, Pinaud R, (2004) Song-induced gene expression: a window on song auditory processing and perception. Ann N Y Acad Sci 1016: 263-281.
23. Mello CV, Pinaud R, Ribeiro S, (1998) Noradrenergic system of the zebra finch brain: immunocytochemical study of dopamine-beta-hydroxylase. Journal of Comparative Neurology 400: 207-228.
24. Mello CV, Ribeiro S, (1998) ZENK protein regulation by song in the brain of songbirds. Journal of Comparative Neurology 393: 426-438.
25. George JM, Clayton DF, (1992) Differential regulation in the avian song control circuit of an mRNA predicting a highly conserved protein related to protein kinase C and the bcr oncogene. Molecular Brain Research 12: 323-329.
26. Holzenberger M, Jarvis ED, Chong C, Grossman M, Nottebohm F, et al. (1997) Selective expression of insulin-like growth factor II in the songbird brain. Journal of Neuroscience 17: 6974-6987.
27. Denisenko-Nehrbass NI, Jarvis E, Scharff C, Nottebohm F, Mello CV, (2000) Site-specific retinoic acid production in the brain of adult songbirds. Neuron 27: 359-370.
28. Mello CV, Jarvis ED, Denisenko N, Rivas M, (1997) Isolation of song-regulated genes in the brain of songbirds. Methods Mol Biol 85: 205-217.
29. Jeong JK, Velho TA, Mello CV, (2005) Cloning and expression analysis of retinoic acid receptors in the zebra finch brain. J Comp Neurol 489: 23-41.
30. Velho TA, Mello CV, (2008) Synapsins are late activity-induced genes regulated by birdsong. J Neurosci 28: 11871-11882.
31. Phan ML, Pytte CL, Vicario DS, (2006) Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. Proc Natl Acad Sci U S A 103: 1088-1093.
32. Mandairon N, Peace S, Karnow A, Kim J, Ennis M, et al. (2008) Noradrenergic modulation in the olfactory bulb influences spontaneous and reward-motivated discrimination, but not the formation of habituation memory. Eur J Neurosci 27: 1210-1219.
33. Gibbs ME, Summers RJ, (2002) Role of adrenoceptor subtypes in memory consolidation. Prog Neurobiol 67: 345-391.
34. Jarvis ED, Mello CV, Nottebohm F, (1995) Associative learning and stimulus novelty influence the song-induced expression of an immediate early gene in the canary forebrain. Learn Mem 2: 62-80.
35. Pinaud R, Terleph TA, Tremere LA, Phan ML, Dagostin AA, et al. (2008) Inhibitory Network Interactions Shape the Auditory Processing of Natural Communication Signals in the Songbird Auditory Forebrain. J Neurophysiol.
36. Moore RY, Bloom FE, (1979) Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems. Annu Rev Neurosci 2: 113-168.
37. 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.
38. Lynch KS, Ball GF, (2008) Noradrenergic deficits alter processing of communication signals in female songbirds. Brain Behav Evol 72: 207-214.
39. Poirier C, Boumans T, Vellema M, De Groof G, Charlier TD, et al. (2011) Own song selectivity in the songbird auditory pathway: suppression by norepinephrine. PLoS One 6: e20131.
40. Pawlisch BA, Stevenson SA, Riters LV, (2011) alpha-Noradrenegic receptor antagonism disrupts female songbird responses to male song. Neurosci Lett 496: 20-24.
41. Berridge CW, Waterhouse BD, (2003) The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42: 33-84.
42. Lindquist JM, Fredriksson JM, Rehnmark S, Cannon B, Nedergaard J, (2000) Beta 3- and alpha1-adrenergic Erk1/2 activation is Src- but not Gi-mediated in Brown adipocytes. J Biol Chem 275: 22670-22677.
43. Strosberg AD, (1993) Structure, function, and regulation of adrenergic receptors. Protein Sci 2: 1198-1209.
44. Sizemore M, Perkel DJ, (2008) Noradrenergic and GABA B receptor activation differentially modulate inputs to the premotor nucleus RA in zebra finches. J Neurophysiol 100: 8-18.
45. Solis MM, Perkel DJ, (2006) Noradrenergic modulation of activity in a vocal control nucleus in vitro. J Neurophysiol 95: 2265-2276.
46. Cardin JA, Schmidt MF, (2004) Noradrenergic inputs mediate state dependence of auditory responses in the avian song system. J Neurosci 24: 7745-7753.
47. 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. J Comp Neurol 366: 613-642.
48. Cheng HY, Clayton DF, (2004) Activation and habituation of extracellular signal-regulated kinase phosphorylation in zebra finch auditory forebrain during song presentation. J Neurosci 24: 7503-7513.
49. Bramham CR, Bacher-Svendsen K, Sarvey JM, (1997) LTP in the lateral perforant path is beta-adrenergic receptor-dependent. Neuroreport 8: 719-724.
50. Huang YY, Kandel ER, (1996) Modulation of both the early and the late phase of mossy fiber LTP by the activation of beta-adrenergic receptors. Neuron 16: 611-617.
51. Huang YY, Martin KC, Kandel ER, (2000) Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. Journal of Neuroscience 20: 6317-6325.
52. Scheiderer CL, Dobrunz LE, McMahon LL, (2004) Novel form of long-term synaptic depression in rat hippocampus induced by activation of alpha 1 adrenergic receptors. J Neurophysiol 91: 1071-1077.
53. Bolhuis JJ, Zijlstra GG, den Boer-Visser AM, Van Der Zee EA, (2000) Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc Natl Acad Sci U S A 97: 2282-2285.
54. London SE, Clayton DF, (2008) Functional identification of sensory mechanisms required for developmental song learning. Nat Neurosci 11: 579-586.
55. McGaugh JL, Roozendaal B, (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12: 205-210.