Social context rapidly modulates the influence of auditory feedback on avian vocal motor control

Journal of Neurophysiology

Volumn 102, Issue 4, 2009, Pages 2485-2497

  Sakata, Jon T ^a   Brainard, Michael S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BIRD; COMPUTER; CONTROLLED STUDY; COURTSHIP; FEEDBACK SYSTEM; FEMALE; FOWL; MALE; MOTOR CONTROL; MOTOR PERFORMANCE; NONHUMAN; PERFORMANCE; PREMOTOR CORTEX; PRIORITY JOURNAL; SOCIAL ENVIRONMENT; SONGBIRD; SPEECH; VOCALIZATION;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY PERCEPTION; FEEDBACK, PSYCHOLOGICAL; FINCHES; MALE; REGRESSION ANALYSIS; SOCIAL BEHAVIOR; SOUND SPECTROGRAPHY; TIME FACTORS; VOCALIZATION, ANIMAL;

EID: 70350325748     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00340.2009     Document Type: Article

References (115)

1. Adams JA. A closed-loop theory of motor learning. J Motor Behav 3: 111-149, 1971.
2. Appeltants D, Absil P, Balthazart J, Ball GF. 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, 2000. (Pubitemid 30138047)
3. Ashmore RC, Wild JM, Schmidt MF. Brainstem and forebrain contributions to the generation of learned motor behaviors for song. J Neurosci 25: 8543-8554, 2005.
4. Ball GF, Castelino CB, Maney DL, Appeltants D, Balthazart J. The activation of birdsong by testosterone: multiple sites of action and role of ascending catecholamine projections. Ann NY Acad Sci 1007: 211-231, 2003.
5. Barclay SR, Harding CF, Waterman SA. Central DSP-4 treatment decreases norepinephrine levels and courtship behavior in male zebra finches. Pharmacol Biochem Behav 53: 213-220, 1996.
6. Berridge KC. Substantia nigra 6-OHDA lesions mimic striatopallidal disruption of syntactic grooming chains: a neural systems analysis of sequence control. Psychobiology 17: 377-385, 1989.
7. Berridge KC, Aldridge JW. Super-stereotypy II: enhancement of a complex movement sequence by intraventricular dopamine D1 agonists. Synapse 37: 205-215, 2000. (Pubitemid 30604924)
8. Berridge KC, Aldridge JW, Houchard KR, Zhuang X. Sequential super-stereotypy of an instinctive fixed action pattern in hyper-dopaminergic mutant mice: a model of obsessive compulsive disorder and Tourette's. BMC Biology 3: 4, 2005. (Pubitemid 41534980)
9. Berridge KC, Fentress JC. Deafferentation does not disrupt natural rules of action syntax. Behav Brain Res 23: 69-76, 1987. (Pubitemid 17234533)
10. Bharati IS, Goodson JL. Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches. Neuroscience 143: 661-670, 2006.
11. Boettiger CA, Doupe AJ. Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning. Neuron 31: 809-818, 2001.
12. Borden GJ. An interpretation of research of feedback interruption in speech. Brain Lang 7: 307-319, 1979.
13. Brainard MS. Contributions of the anterior forebrain pathway to vocal plasticity. Ann NY Acad Sci 1016: 377-394, 2004.
14. Brainard MS, Doupe AJ. Auditory feedback in learning and maintenance of vocal behaviour. Nat Rev Neurosci 1: 31-40, 2000a.
15. Brainard MS, Doupe AJ. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404: 762-766, 2000b.
16. Brainard MS, Doupe AJ. Postlearning consolidation of birdsong: stabilizing effects of age and anterior forebrain lesions. J Neurosci 21: 2501-2517, 2001.
17. Brainard MS, Doupe AJ. What songbirds teach us about learning. Nature 417: 351-358, 2002.
18. Brumm H, Slater PJB. Animals can vary signal amplitude with receiver distance: evidence from zebra finch song. Anim Behav 72: 699-705, 2006. (Pubitemid 44311119)
19. Cardin JA, Schmidt MF. Noradrenergic inputs mediate state dependence of auditory responses in the avian song system. J Neurosci 24: 7745-7753, 2004.
20. Castelino CB, Ball GF. A role for norepinephrine in the regulation of context-dependent ZENK expression in male zebra finches (Taeniopygia guttata). Eur J Neurosci 21: 1962-1972, 2005.
21. Castelino CB, Diekamp B, Ball GF. Noradrenergic projections to the song control nucleus Area X of the medial striatum in male zebra finches (Taeniopygia guttata). J Comp Neurol 502: 544-562, 2007.
22. Cowie R, Douglas-Cowie E. Postlingually Acquired Deafness: Speech Deterioration and the Wider Consequences. Berlin: Mouton de Gruyter, 1992.
23. Cromwell HC, Berridge KC, Drago J, Levine MS. Action sequencing is impaired in D1A-deficient mutant mice. Eur J Neurosci 10: 2426-2432, 1998. (Pubitemid 128707695)
24. Cynx J. Experimental determination of a unit of song production in the zebra finch (Taeniopygia guttata). J Comp Psychol 104: 3-10, 1990.
25. Cynx J, Lewis R, Tavel B, Tse H. Amplitude regulation of vocalizations in noise by a songbird, Taeniopygia guttata. Anim Behav 56: 107-113, 1998.
26. Cynx J, von Rad U. Immediate and transitory effects of delayed auditory feedback on bird song production. Anim Behav 62: 305-312, 2001. (Pubitemid 32792876)
27. Dave AS, Yu AC, Margoliash D. Behavioral state modulation of auditory activity in a vocal motor system. Science 282: 2250-2254, 1998. (Pubitemid 29004071)
28. Derégnaucourt S, Mitra PP, Fehér O, Pytte C, Tchernichovski O. How sleep affects the developmental learning of bird song. Nature 433: 710-716, 2005. (Pubitemid 40292973)
29. Doupe AJ, Kuhl PK. Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 22: 567-631, 1999.
30. Doya K, Sejnowski TJ. A computational model of avian song learning. In: The New Cognitive Neurosciences, edited by Gazzaniga M. Cambridge, MA: MIT Press, 2000, p. 469-482.
31. Doyon J, Benali H. Reorganization and plasticity in the adult brain during learning of motor skills. Curr Opin Neurobiol 15: 161-167, 2005. (Pubitemid 41569264)
32. Fee MS, Kozhevnikov AA, Hahnloser RH. Neural mechanisms of vocal sequence generation in the songbird. Ann NY Acad Sci 1016: 153-170, 2004.
33. Franz M, Goller F. Respiratory units of motor production and song imitation in the zebra finch. J Neurobiol 51: 129-141, 2002.
34. Gil D, Slater PJB. Song organization and singing patterns of the willow warbler, Phylloscopus trochilus. Behaviour 137: 759-782, 2000.
35. Hahnloser RH, Kozhevnikov AA, Fee MS. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419: 65-70, 2002.
36. Hampton CM, Sakata JT, Brainard MS. An avian basal ganglia-forebrain circuit contributes differentially to syllable versus sequence variability of adult Bengalese finch song. J Neurophysiol 101: 3235-3245, 2009.
37. Hara E, Kubikova L, Hessler NA, Jarvis ED. Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context. Eur J Neurosci 25: 3406-3416, 2007.
38. Harding CF, Barclay SR, Waterman SA. Changes in catecholamine levels and turnover rates in hypothalamic, vocal control, and auditory nuclei in male zebra finches during development. J Neurobiol 34: 329-346, 1998.
39. Hessler NA, Doupe AJ. Social context modulates singing-related neural activity in the songbird forebrain. Nat Neurosci 2: 209-211, 1999.
40. Horita H, Wada K, Jarvis ED. Early onset of deafening-induced song deterioration and differential requirements of the pallial-basal ganglia vocal pathway. Eur J Neurosci 28: 2519-2532, 2008.
41. Houde JF, Jordan MI. Sensorimotor adaptation in speech production. Science 279: 1213-1216, 1998.
42. Howell P, Archer A. Susceptibility to the effects of delayed auditory feedback. Percept Psychophys 36: 296-302, 1984.
43. Howell P, Barry W, Vinson D. Strength of British English accents in altered listening conditions. Percept Psychophys 68: 139-153, 2006.
44. Howell P, Dworzynski K. Strength of German accent under altered auditory feedback. Percept Psychophys 63: 501-513, 2001.
45. Howell P, Powell DJ. Delayed auditory feedback with delayed sounds varying in duration. Percept Psychophys 42: 166-172, 1987.
46. Iyengar S, Viswanathan SS, Bottjer SW. Development of topography within song control circuitry of zebra finches during the sensitive period for song learning. J Neurosci 19: 6037-6057, 1999.
47. Jarvis ED, Scharff C, Grossman MR, Ramos JA, Nottebohm F. For whom the bird sings: context-dependent gene expression. Neuron 21: 775-788, 1998. (Pubitemid 28498786)
48. Kao MH, Brainard MS. Lesions of an avian basal ganglia circuit prevent context-dependent changes to song variability. J Neurophysiol 96: 1441-1455, 2006.
49. Kao MH, Doupe AJ, Brainard MS. Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433: 638-643, 2005.
50. Kao MH, Wright BD, Doupe AJ. Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context. J Neurosci 28: 13232-13247, 2008.
51. Keller GB, Hahnloser RH. Neural processing of auditory feedback during vocal practice in a songbird. Nature 457: 187-190, 2009.
52. Kobayashi KI, Okanoya K. Context-dependent song amplitude control in Bengalese finches. Neuroreport 14: 521-524, 2003. (Pubitemid 36337963)
53. Konishi M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z Tierpsychol 22: 770-783, 1965.
54. Konishi M. The role of auditory feedback in birdsong. Ann NY Acad Sci 1016: 463-475, 2004.
55. Konishi M, Nottebohm F. Experimental studies in the ontogeny of avian vocalizations. In: Bird Vocalizations, edited by Hinde RA. Cambridge, England: Cambridge, 1969, p. 29-48.
56. Kozhevnikov A, Fee MS. Singing-related activity of identified HVC neurons in the zebra finch. J Neurophysiol 97: 4271-4283, 2007. (Pubitemid 47080656)
57. Lane H, Webster JW. Speech deterioration in postlingually deafened adults. J Acoust Soc Am 89: 859-866, 1991.
58. Lee BS. Effects of delayed speech feedback. J Acoust Soc Am 22: 824-826, 1950.
59. Leonardo A. Experimental test of the birdsong error-correction model. Proc Natl Acad Sci USA 101: 16935-16940, 2004. (Pubitemid 39601342)
60. Leonardo A, Konishi M. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399: 466-470, 1999. (Pubitemid 29258851)
61. Li R, Sakaguchi H. Cholinergic innervation of the song control nuclei by the ventral paleostriatum in the zebra finch: a double-labeling study with retrograde fluorescent tracers and choline acetyltransferase immunohistochemistry. Brain Res 763: 239-246, 1997. (Pubitemid 27364444)
62. Livingston FS, Mooney R. Development of intrinsic and synaptic properties in a forebrain nucleus essential to avian song learning. J Neurosci 17: 8997-9009, 1997. (Pubitemid 27498428)
63. Lombardino AJ, Nottebohm F. Age at deafening affects the stability of learned song in adult male zebra finches. J Neurosci 20: 5054-5064, 2000. (Pubitemid 30421709)
64. Long MA, Fee MS. Using temperature to analyse temporal dynamics in the songbird motor pathway. Nature 456: 189-194, 2008.
65. MacKay DG. Metamorphosis of a critical interval: age-linked changes in the delay in auditory feedback that produces maximal disruption of speech. J Acoust Soc Am 43: 811-821, 1968.
66. Manabe K, Sadr EI, Dooling RJ. Control of vocal intensity in budgerigars (Melopsittacus undulatus): differential reinforcement of vocal intensity and the Lombard effect. J Acoust Soc Am 103: 1190-1198, 1998. (Pubitemid 28087588)
67. Maney DL, Ball GF. Fos-like immunoreactivity in catecholaminergic brain nuclei after territorial behavior in free-living song sparrows. J Neurobiol 56: 163-170, 2003.
68. Miller CT, Flusberg S, Hauser MD. Interruptibility of long call production in tamarins: implications for vocal control. J Exp Biol 206: 2629-2639, 2003. (Pubitemid 37042042)
69. Mooney R. Synaptic mechanisms for auditory-vocal integration and the correction of vocal errors. Ann NY Acad Sci 1016: 476-494, 2004. (Pubitemid 38951482)
70. Morris D. The reproductive behavior of the zebra finch (Poephila guttata), with special reference to pseudofemale behaviour and displacement activities. Behaviour 7: 271-321, 1954.
71. Nordeen KW, Nordeen EJ. Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav Neural Biol 57: 58-66, 1992.
72. Nottebohm F, Stokes TM, Leonard CM. Central control of song in the canary, Serinus canarius. J Comp Neurol 165: 457-486, 1976.
73. Okanoya K, Yamaguchi A. Adult Bengalese finches (Lonchura striata var. domestica) require real-time auditory feedback to produce normal song syntax. J Neurobiol 33: 343-356, 1997. (Pubitemid 27411216)
74. Ölveckzy BP, Andalman AS, Fee MS. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biology 3: e153, 2005.
75. Pearson KG. Generating the walking gait: role of sensory feedback. Prog Brain Res 143: 123-129, 2004.
76. Prather JF, Peters S, Nowicki S, Mooney R. Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 451: 305-310, 2008.
77. Pratt J, Chasteen AL, Abrams RA. Rapid aimed limb movements: age differences and practice effects in component submovements. Psychol Aging 9: 325-334, 1994. (Pubitemid 24279832)
78. Price PH. Developmental determinants of structure in zebra finch song. J Comp Physiol Psychol 93: 268-277, 1979.
79. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Durand S, Gunturkun O, Lee DW, Mello CV, Powers A, White SA, Hough G, Kubikova L, Smulders TV, Wada K, Dugas-Ford J, Husband S, Yamamoto K, Yu J, Siang C, Jarvis ED. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473: 377-414, 2004.
80. Riebel K, Todt D. Light flash stimulation alters the nightingale's singing style: implications for song control mechanisms. Behavior 134: 789-808, 1997. (Pubitemid 127107964)
81. Riters LV, Alger SJ. Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: possible neural substrates for sexually motivated song. Cell Tissue Res 316: 35-44, 2004.
82. Sabes PN. The planning and control of reaching movements. Curr Opin Neurobiol 10: 740-746, 2000.
83. Sakata JT, Brainard MS. Real-time contributions of auditory feedback to avian vocal motor control. J Neurosci 26: 9619-9628, 2006.
84. Sakata JT, Brainard MS. Online contributions of auditory feedback to neural activity in avian song control circuitry. J Neurosci 28: 11378-11390, 2008.
85. Sakata JT, Hampton CM, Brainard MS. Social modulation of sequence and syllable variability in adult birdsong. J Neurophysiol 99: 1700-1711, 2008.
86. Sasaki A, Sotnikova TD, Gainetdinov RR, Jarvis ED. Social context-dependent singing-regulated dopamine. J Neurosci 26: 9010-9014, 2006.
87. Schmidt RA. A schema theory of discrete motor learning skill. Psychol Rev 82: 225-260, 1975.
88. Schultz W, Dickinson A. Neuronal coding of prediction errors. Annu Rev Neurosci 23: 473-500, 2000.
89. Scott LL, Nordeen EJ, Nordeen KW. LMAN lesions prevent song degradation after deafening without reducing HVC neuron addition. Dev Neurobiol 67: 1407-1418, 2007.
90. Seki Y, Suzuki K, Takahasi M, Okanoya K. Song motor control organizes acoustic patterns on two levels in Bengalese finches (Lonchura striata var. domestica). J Comp Physiol [A] 194: 533-543, 2008.
91. Shea SD, Margoliash D. Basal forebrain cholinergic modulation of auditory activity in the zebra finch song system. Neuron 40: 1213-1226, 2003. (Pubitemid 38032796)
92. Smotherman MS. Sensory feedback control of mammalian vocalizations. Behav Brain Res 182: 315-326, 2007.
93. Sober SJ, Brainard MS. Adult birdsong is actively maintained by error correction. Nat Neurosci 12: 927-931, 2009.
94. Soha JA, Shimizu T, Doupe AJ. Development of the catecholaminergic innervation of the song system of the male zebra finch. J Neurobiol 29: 473-489, 1996. (Pubitemid 26095496)
95. Sossinka R, Böhner J. Song types in the zebra finch Poephila guttata castanotis. Z Tierpsychol 53: 123-132, 1980.
96. Suthers RA, Goller F, Wild JM. Somatosensory feedback modulates the respiratory motor program of crystallized birdsong. Proc Natl Acad Sci USA 99: 5680-5685, 2002. (Pubitemid 34411610)
97. Sutton RS, Barto AG. Reinforcement Learning: An Introduction. Cambridge, MA: MIT Press, 1998.
98. Tchernichovski O, Mitra PP, Lints T, Nottebohm F. Dynamics of the vocal imitation process: how a zebra finch learns its song. Science 291: 2564-2569, 2001. (Pubitemid 32249674)
99. ten Cate C, Ballintijn MR. Dove coos and flashed lights: interruptibility of "song" in a nonsongbird. J Comp Psychol 110: 267-275, 1996.
100. Teramitsu I, White SA. FoxP2 regulation during undirected singing in adult songbirds. J Neurosci 26: 7390-7394, 2006. (Pubitemid 44315207)
101. Todorov E, Jordan MI. Optimal feedback control as a theory of motor coordination. Nat Neurosci 5: 1226-1235, 2002. (Pubitemid 35247183)
102. Troyer TW, Doupe AJ. An associational model of birdsong sensorimotor learning. I. Efference copy and the learning of song syllables. J Neurophysiol 84: 1204-1223, 2000. (Pubitemid 30688147)
103. Tumer EM, Brainard MS. Performance variability enables adaptive plasticity of crystallized adult birdsong. Nature 450: 1240-1244, 2007.
104. Van Borsel J, Sunaert R, Engelen S. Speech disruption under delayed auditory feedback in multilingual speakers. J Fluency Disord 30: 201-217, 2005. (Pubitemid 41218588)
105. Vu ET, Mazurek ME, Kuo YC. Identification of a forebrain motor programming network for the learned song of zebra finches. J Neurosci 14: 6924-6934, 1994.
106. Wang CZ, Herbst JA, Keller GB, Hahnloser RH. Rapid interhemispheric switching during vocal production in a songbird. PLoS Biol 6: e250, 2008.
107. Webster FL, Dorman MF. Changes in reliance on auditory feedback cues as a function of oral practice. J Speech Hear Res 14: 307-311, 1971.
108. Williams H, Connor DM, Hill JW. Testosterone decreases the potential for song plasticity in adult male zebra finches. Horm Behav 44: 402-412, 2003. (Pubitemid 37476427)
109. Woolley SC, Doupe AJ. Social context-induced song variation affects female behavior and gene expression. PLoS Biol 6: e62, 2008.
110. Woolley SM, Rubel EW. Bengalese finches Lonchura Striata domestica depend upon auditory feedback for the maintenance of adult song. J Neurosci 17: 6380-6390, 1997. (Pubitemid 27329910)
111. Wyke BD. Laryngeal neuromuscular control systems in singing. A review of current concepts. Folia Phoniatr (Basel) 26: 295-306, 1974.
112. Yanagihara S, Hessler NA. Modulation of singing-related activity in the songbird ventral tegmental area by social context. Eur J Neurosci 24: 3619-3627, 2006. (Pubitemid 44952627)
113. Yu AC, Margoliash D. Temporal hierarchical control of singing in birds. Science 273: 1871-1875, 1996.
114. Zann RA. The Zebra Finch: A Synthesis of Field and Laboratory Studies. Oxford, UK: Oxford, 1996.
115. Zatare JM, Zatorre RJ. Experience-dependent neural substrates involved in vocal pitch regulation during singing. Neuroimage 40: 1871-1887, 2008.