From songs to synapses: Molecular mechanisms of birdsong memory

BioEssays

Volumn 33, Issue 5, 2011, Pages 377-385

  Moorman, Sanne ^a   Mello, Claudio V ^b   Bolhuis, Johan J ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Birdsong; Genes; Learning; Memory; Synapse

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; GLUTAMATE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; SYNAPSIN;

AUDITORY MEMORY; DENDRITE; GENE EXPRESSION; GENETIC DATABASE; HIPPOCAMPUS; HUMAN; IMMEDIATE EARLY GENE; LEARNING; MEMORY; MOLECULAR BIOLOGY; NERVE CELL; NONHUMAN; PLASTICITY; REVIEW; SIGNAL TRANSDUCTION; SONGBIRD; SYNAPSE;

ANIMALS; BRAIN; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENES, IMMEDIATE-EARLY; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION; SONGBIRDS; SYNAPSINS; VOCALIZATION, ANIMAL;

AVES; MAMMALIA; PASSERI; TAENIOPYGIA GUTTATA;

EID: 79954588607     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201000150     Document Type: Review

References (108)

1. Bolhuis JJ, Okanoya K, Scharff C. 2010. Twitter evolution: converging mechanisms in birdsong and human speech. Nat Rev Neurosci 11: 747-59.
2. Hauser MD, Chomsky N, Fitch WT. 2002. The faculty of language: what is it, who has it, and how did it evolve? Science 298: 1569-79.
3. Bolhuis JJ, Wynne CD. 2009. Can evolution explain how minds work? Nature 458: 832-3.
4. Bolhuis JJ, Eda-Fujiwara H. 2010. Birdsong and the brain: the syntax of memory. Neuroreport 21: 395-8.
5. Jarvis ED, Mello CV. 2000. Molecular mapping of brain areas involved in parrot vocal communication. J Comp Neurol 419: 1-31.
6. Jarvis ED, Ribeiro S, da Silva ML, Ventura D, et al. 2000. Behaviourally driven gene expression reveals song nuclei in hummingbird brain. Nature 406: 628-32.
7. Nottebohm F. 1972. The origins of vocal learning. Am Nat 106: 116-40.
8. Maul KK, Voss HU, Parra LC, Salgado-Commissariat D, et al. 2010. The development of stimulus-specific auditory responses requires song exposure in male but not female zebra finches. Dev Neurobiol 70: 28-40.
9. Bolhuis JJ, Gahr M. 2006. Neural mechanisms of birdsong memory. Nat Rev Neurosci 7: 347-57.
10. Doupe AJ, Kuhl PK. 1999. Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 22: 567-631.
11. Mooney R. 2009. Neurobiology of song learning. Curr Opin Neurobiol 19: 654-60.
12. Reiner A, Perkel DJ, Mello CV, Jarvis ED. 2004. Song birds and the revised avian brain nomenclature. Ann NY Acad Sci 1016: 77-108.
13. Jarvis E, Güntürkün O, Bruce L, Csillag A, et al. 2005. Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6: 151-9.
14. Vicario DS. 1991. Organization of the zebra finch song control system: functional organization of outputs from nucleus robustus archistriatalis. J Comp Neurol 309: 486-94.
15. Bottjer SW, Halsema KA, Brown SA, Miesner EA. 1989. Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J Comp Neurol 279: 312-26.
16. Luo M, Ding L, Perkel DJ. 2001. An avian basal ganglia pathway essential for vocal learning forms a closed topographic loop. J Neurosci 21: 6836-45.
17. Vates GE, Vicario DS, Nottebohm F. 1997. Reafferent thalamo-'cortical' loops in the song system of oscine songbirds. J Comp Neurol 380: 275-90.
18. Nottebohm F, Stokes TM, Leonard CM. 1976. Central control of song in the canary, Serinus canarius J Comp Neurol 165: 457-86.
19. Bottjer SW, Miesner EA, Arnold AP. 1984. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224: 901-3.
20. Scharff C, Nottebohm F. 1991. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J Neurosci 11: 2896-913.
21. Brainard MS, Doupe AJ. 2000. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404: 762-6.
22. Olveczky BP, Andalman AS, Fee MS. 2005. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol 3: e153.
23. Brenowitz EA. 1997. Comparative approaches to the avian song system. J Neurobiol 33: 517-31.
24. Doupe AJ, Perkel DJ, Reiner A, Stern EA. 2005. Birdbrains could teach basal ganglia research a new song. Trends Neurosci 28: 353-63.
25. Roberts TF, Klein ME, Kubke MF, Wild JM, et al. 2008. Telencephalic neurons monosynaptically link brainstem and forebrain premotor networks necessary for song. J Neurosci 28: 3479-89.
26. Bolhuis JJ. 2008. Chasin' the trace: the neural substrate of bird song memory. In Zeigler HP, Marler P, eds; Neuroscience of Birdsong. CUP: Cambridge. 269-279.
27. Zeigler HP, Marler P, eds. 2008. Neuroscience of Birdsong. CUP: Cambridge.
28. Mello CV, Velho TA, Pinaud R. 2004. Song-induced gene expression: a window on song auditory processing and perception. Ann NY Acad Sci 1016: 263-81.
29. Mello CV. 2004. Gene regulation by song in the auditory telencephalon of songbirds. Front Biosci 9: 63-73.
30. Fortune ES, Margoliash D. 1992. Cytoarchitectonic organization and morphology of cells of the field L complex in male zebra finches (Taenopygia guttata). J Comp Neurol 325: 388-404.
31. Mello CV, Vates GE, Okuhata S, Nottebohm F. 1998. Descending auditory pathways in the adult male zebra finch (Taeniopygia guttata). J Comp Neurol 395: 137-60.
32. 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: 613-42.
33. Mello CV, Vicario DS, Clayton DF. 1992. Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci USA 89: 6818-22.
34. Mello CV, Clayton DF. 1994. Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J Neurosci 14: 6652-66.
35. Mello C, Nottebohm F, Clayton D. 1995. Repeated exposure to one song leads to a rapid and persistent decline in an immediate early gene's response to that song in zebra finch telencephalon. J Neurosci 15: 6919-25.
36. Velho TA, Pinaud R, Rodrigues PV, Mello CV. 2005. Co-induction of activity-dependent genes in songbirds. Eur J Neurosci 22: 1667-78.
37. Chew SJ, Mello C, Nottebohm F, Jarvis E, et al. 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 USA 92: 3406-10.
38. Chew SJ, Vicario DS, Nottebohm F. 1996. A large-capacity memory system that recognizes the calls and songs of individual birds. Proc Natl Acad Sci USA 93: 1950-5.
39. Gentner TQ, Margoliash D. 2003. Neuronal populations and single cells representing learned auditory objects. Nature 424: 669-74.
40. 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 USA 103: 1088-93.
41. Stripling R, Volman SF, Clayton DF. 1997. Response modulation in the zebra finch neostriatum: relationship to nuclear gene regulation. J Neurosci 17: 3883-93.
42. Terleph TA, Mello CV, Vicario DS. 2006. Auditory topography and temporal response dynamics of canary caudal telencephalon. J Neurobiol 66: 281-92.
43. Wild JM, Karten HJ, Frost BJ. 1993. Connections of the auditory forebrain in the pigeon (Columba livia). J Comp Neurol 337: 32-62.
44. Hahnloser RH, Kotowicz A. 2010. Auditory representations and memory in birdsong learning. Curr Opin Neurobiol 20: 332-9.
45. Theunissen FE, Shaevitz SS. 2006. Auditory processing of vocal sounds in birds. Curr Opin Neurobiol 16: 400-7.
46. Li X, Wang X, Tannenhauser J, Podell S, et al. 2007. Genomic resources for songbird research and their use in characterizing gene expression during brain development. Proc Natl Acad Sci USA 104: 6833-9.
47. Lovell PV, Clayton DF, Replogle KL, Mello CV. 2008. Birdsong "transcriptomics": neurochemical specializations of the oscine song system. PLoS One 3: e3440.
48. Wada K, Howard JT, McConnell P, Whitney O, et al. 2006. A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc Natl Acad Sci USA 103: 15212-7.
49. Thompson JV, Gentner TQ. 2010. Song recognition learning and stimulus-specific weakening of neural responses in the avian auditory forebrain. J Neurophysiol 103: 1785-97.
50. Pittenger C, Kandel ER. 2003. In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus. Philos Trans R Soc Lond B Biol Sci 358: 757-63.
51. Dong S, Replogle KL, Hasadsri L, Imai BS, et al. 2009. Discrete molecular states in the brain accompany changing responses to a vocal signal. Proc Natl Acad Sci USA 106: 11364-9.
52. Bolhuis JJ, Zijlstra GGO, 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 USA 97: 2282-5.
53. Bolhuis JJ, Hetebrij E, Den Boer-Visser AM, De Groot JH, et al. 2001. Localized immediate early gene expression related to the strength of song learning in socially reared zebra finches. Eur J Neurosci 13: 2165-70.
54. Terpstra NJ, Bolhuis JJ, den Boer-Visser AM. 2004. An analysis of the neural representation of birdsong memory. J Neurosci 24: 4971-7.
55. Gobes SMH, Zandbergen MA, Bolhuis JJ. 2010. Memory in the making: localized brain activation related to song learning in young songbirds. Proc Roy Soc B 277: 3343-51.
56. Riebel K, Smallegange IM, Terpstra NJ, Bolhuis JJ. 2002. Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc Roy Soc B 269: 729-33.
57. Terpstra NJ, Bolhuis JJ, Riebel K, Van Der Burg JMM, et al. 2006. Localized brain activation specific to auditory memory in a female songbird. J Comp Neurol 494: 784-91.
58. London SE, Clayton DF. 2008. Functional identification of sensory mechanisms required for developmental song learning. Nat Neurosci 11: 579-86.
59. Gobes SM, Bolhuis JJ. 2007. Birdsong memory: a neural dissociation between song recognition and production. Curr Biol 17: 789-93.
60. Velho TAF, Mello CV. 2008. Transcriptional regulation of activity-dependent genes by birdsong. In Dudek SM, ed; Transcriptional Regulation by Neuronal Activity: To the Nucleus and Back. New York, NY: Springer. p 3-26.
61. Farivar R, Zangenehpour S, Chaudhuri A. 2004. Cellular-resolution activity mapping of the brain using immediate-early gene expression. Front Biosci 9: 104-9.
62. Sagar SM, Sharp FR, Curran T. 1988. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240: 1328-31.
63. Mello CV, Ribeiro S. 1998. ZENK protein regulation by song in the brain of songbirds. J Comp Neurol 393: 426-38.
64. Mello CV. 2002. Mapping vocal communication pathways in birds with inducible gene expression. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 188: 943-59.
65. Ribeiro S, Cecchi GA, Magnasco MO, Mello CV. 1998. Toward a song code: evidence for a syllabic representation in the canary brain. Neuron 21: 359-71.
66. Horn G. 2004. Pathways of the past: the imprint of memory. Nat Rev Neurosci 5: 108-20.
67. McCabe BJ, Nicol AU. 1999. The recognition memory of imprinting: biochemistry and electrophysiology. Behav Brain Res 98: 253-60.
68. Leitner S, Voigt C, Metzdorf R, Catchpole CK. 2005. Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J Neurobiol 64: 275-84.
69. Steward O, Worley P. 2002. Local synthesis of proteins at synaptic sites on dendrites: role in synaptic plasticity and memory consolidation? Neurobiol Learn Mem 78: 508-27.
70. Bramham CR, Alme MN, Bittins M, Kuipers SD, et al. 2010. The Arc of synaptic memory. Exp Brain Res 200: 125-40.
71. Messaoudi E, Kanhema T, Soulé J, Tiron A, et al. 2007. Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J Neurosci 27: 10445-55.
72. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, 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.
73. Horita H, Wada K, Rivas MV, Hara E, et al. 2010. The dusp1 immediate early gene is regulated by natural stimuli predominantly in sensory input neurons. J Comp Neurol 518: 2873-901.
74. Patterson KI, Brummer T, O'Brien PM, Daly RJ. 2009. Dual-specificity phosphatases: critical regulators with diverse cellular targets. Biochem J 418: 475-89.
75. Mello CV, Clayton DF. 1995. Differential induction of the ZENK gene in the avian forebrain and song control circuit after metrazole-induced depolarization. J Neurobiol 26: 145-61.
76. Halazonetis TD, Georgopoulos K, Greenberg ME, Leder P. 1988. C-Jun dimerizes with itself and with c-Fos, forming complexes of different DNA binding affinities. Cell 55: 917-24.
77. Sung Y-J, Wu F, Schacher S, Ambron RT. 2006. Synaptogenesis regulates axotomy-induced activation of c-Jun-activator protein-1 transcription. J Neurosci 26: 6439-49.
78. Nastiuk KL, Mello CV, George JM, Clayton DF. 1994. Immediate-early gene responses in the avian song control system: cloning and expression analysis of the canary c-jun cDNA. Mol Brain Res 27: 299-309.
79. Jin H, Clayton DF. 1997. Localized changes in immediate-early gene regulation during sensory and motor learning in zebra finches. Neuron 19: 1049-59.
80. Mello CV. 2004. Identification and analysis of vocal communication pathways in birds through inducible gene expression. An Acad Bras Cienc 76: 243-6.
81. Bailey DJ, Wade J. 2003. Differential expression of the immediate early genes FOS and ZENK following auditory stimulation in the juvenile male and female zebra finch. Mol Brain Res 116: 147-54.
82. Duffy DL, Bentley GE, Ball GF. 1999. Does sex or photoperiodic condition influence ZENK induction in response to song in European starlings? Brain Res 844: 78-82.
83. Vignal C, Attia J, Mathevon N, Beauchaud M. 2004. Background noise does not modify song-induced genic activation in the bird brain. Behav Brain Res 153: 241-8.
84. Vignal C, Andru J, Mathevon N. 2005. Social context modulates behavioural and brain immediate early gene responses to sound in male songbird. Eur J Neurosci 22: 949-55.
85. Jarvis ED, Nottebohm F. 1997. Motor-driven gene expression. Proc Natl Acad Sci USA 94: 4097-102.
86. Jones MW, Errington ML, French PJ, Fine A, et al. 2001. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4: 289-96.
87. Stripling R, Kruse AA, Clayton DF. 2001. Development of song responses in the zebra finch caudomedial neostriatum: role of genomic and electrophysiological activities. J Neurobiol 48: 163-80.
88. Velho TAF, Mello CV. 2008. Synapsins are late activity-induced genes regulated by birdsong. J Neurosci 28: 11871-82.
89. Evergren E, Benfenati F, Shupliakov O. 2007. The synapsin cycle: a view from the synaptic endocytic zone. J Neurosci Res 85: 2648-56.
90. Ferreira A, Han HQ, Greengard P, Kosik KS. 1995. Suppression of synapsin II inhibits the formation and maintenance of synapses in hippocampal culture. Proc Natl Acad Sci USA 92: 9225-9.
91. Han H, Nichols RA, Rubin MR, Bahler M, et al. 1991. Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb. Nature 349: 697-700.
92. Matsunaga E, Okanoya K. 2008. Expression analysis of cadherins in the songbird brain: relationship to vocal system development. J Comp Neurol 508: 329-42.
93. Replogle K, Arnold AP, Ball GF, Band M, et al. 2008. The songbird neurogenomics (SoNG) initiative: community-based tools and strategies for study of brain gene function and evolution. BMC Genomics 9: 131.
94. Wade J, Peabody C, Coussens P, Tempelman RJ, et al. 2004. A cDNA microarray from the telencephalon of juvenile male and female zebra finches. J Neurosci Methods 138: 199-206.
95. Pinaud R, Velho TA, Jeong JK, Tremere LA, et al. 2004. GABAergic neurons participate in the brain's response to birdsong auditory stimulation. Eur J Neurosci 20: 1318-30.
96. Pinaud R, Mello CV. 2007. GABA immunoreactivity in auditory and song control brain areas of zebra finches. J Chem Neuroanat 34: 1-21.
97. Morris RGM. 2006. Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 23: 2829-46.
98. Wada K, Sakaguchi H, Jarvis ED, Hagiwara M. 2004. Differential expression of glutamate receptors in avian neural pathways for learned vocalization. J Comp Neurol 476: 44-64.
99. Ramirez-Amaya V. 2007. Molecular mechanisms of synaptic plasticity underlying long-term memory formation - neural plasticity and memory. In Bermúdez-Rattoni F, ed; Neural Plasticity and Memory: From Genes to Brain Imaging. Boca Raton, FL: CRC Press. p 47-66.
100. Basham ME, Nordeen EJ, Nordeen KW. 1996. Blockade of NMDA receptors in the anterior forebrain impairs sensory acquisition in the zebra finch (Poephila guttata). Neurobiol Learn Mem 66: 295-304.
101. Aamodt SM, Nordeen EJ, Nordeen KW. 1996. Blockade of NMDA receptors during song model exposure impairs song development in juvenile zebra finches. Neurobiol Learn Mem 65: 91-8.
102. 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: 7503-13.
103. Ying S, Futter M, Rosenblum K, Webber MJ, et al. 2002. Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci 22: 1532-40.
104. Sweatt JD. 2001. The neuronal MAP kinase cascade: a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76: 1-10.
105. Cingolani LA, Goda Y. 2008. Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9: 344-56.
106. McGaugh JL. 2000. Memory - A century of consolidation. Science 287: 248-51.
107. White SA. 2010. Genes and vocal learning. Brain Lang 115: 21-8.
108. Agate RJ, Scott BB, Haripal B, Lois C, et al. 2009. Transgenic songbirds offer an opportunity to develop a genetic model for vocal learning. Proc Natl Acad Sci USA 106: 17963-7.