Cellular, circuit, and synaptic mechanisms in song learning

Annals of the New York Academy of Sciences

Volumn 1016, Issue , 2004, Pages 495-523

  Doupe, Allison J ^a   Solis, Michele M ^a,b   Kimpo, Rhea ^a,c   Boettiger, Charlotte A ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

Author keywords

Bird's own song; Correlation; Critical period; Interconnectivity; Network; NMDA receptor; Plasticity; Recurrent; Selectivity; Sensorimotor; Spike timing dependence; Template; Tutor; Variability

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AUDITORY MEMORY; BASAL GANGLION; BEHAVIOR; BIRD; CELL ACTIVITY; CELL FUNCTION; CELL POPULATION; CONFERENCE PAPER; CORRELATION ANALYSIS; DATA ANALYSIS; ELECTROPHYSIOLOGY; FOREBRAIN; HEARING; LEARNING; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; NONLINEAR SYSTEM; SENSORIMOTOR CORTEX; SENSORIMOTOR FUNCTION; SINGING; SLEEP; SONGBIRD; SOUND DETECTION; STIMULUS RESPONSE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; TOPOGRAPHY; WAKEFULNESS;

AVES; BOS; PASSERI;

EID: 3242730199     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1196/annals.1298.035     Document Type: Conference Paper

References (109)

1. DOUPE, A.J. & P.K. KUHL. 1999. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22: 567-631.
2. WALDSTEIN, R.S. 1990. Effects of postlingual deafness on speech production: implications for the role of auditory feedback. J. Acoust. Soc. Am. 88: 2099-2144.
3. KONISHI, M. 1965. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 22: 770-783.
4. NORDEEN, K.W. & E.J. NORDEEN. 1992. Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav. Neural. Biol. 57: 58-66.
5. PRICE, P.H. 1979. Developmental determinants of structure in zebra finch song. J. Comp. Phys. Psych. 93: 268-277.
6. MARLER, P. 1970. A comparative approach to vocal learning: song development in white-crowned sparrows. J. Comp. Phys. Pyschol. 71: 1-25.
7. IMMELMANN, K. 1969. Song development in the zebra finch and other estrildid finches. In Bird Vocalizations. R.A. Hinde, Ed.: 61-74. Cambridge University Press. London.
8. EALES, L.A. 1985. Song learning in zebra finches: some effects of song model availability on what is learnt and when. Anim. Behav. 33: 1293-1300.
9. NORDEEN, E.J. & K.W. NORDEEN. 1992. Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav. Neural Biol. 57: 58-66.
10. LEONARDO, A. & M. KONISHI. 1999. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399: 466-470.
11. NOTTEBOHM, F., T.M. STOKES & A.P. ARNOLD. 1976. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165: 457-486.
12. BOTTJER, S.W., E.A. MIESNER & A.P. ARNOLD. 1984. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224: 901-903.
13. SOHRABJI, F., E.J. NORDEEN & K.W. NORDEEN. 1990. Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behav. Neural. Biol. 53: 51-63.
14. SCHARFF, C. & F. NOTTEBOHM. 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: 2896-2913.
15. WILLIAMS, H. & N. MEHTA. 1999. Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production. J. Neurobiol. 39: 14-28.
16. BRAINARD, M.S. & A.J. DOUPE. 2000. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404: 762-766.
17. BRAINARD, M.S. & A.J. DOUPE. 2000. Auditory feedback in learning and maintenance of vocal behavior. Nat. Rev. Neurosci. 1: 31-40.
18. MCCASLAND, J.S. & M. KONISHI. 1981. Interactions between auditory and motor activities in an avian song control nucleus. Proc. Natl. Acad. Sci. USA 78: 7815-7819.
19. MARGOLIASH, D. 1983. Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J. Neurosci. 3: 1039-1057.
20. DOUPE, A.J. & M. KONISHI. 1991. Song-selective auditory circuits in the vocal control system of the zebra finch. Proc. Natl. Acad. Sci. USA 88: 11339-11343.
21. DAVE, A.S. & D. MARGOLIASH. 2000. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290: 812-816.
22. SOLIS, M. & A. DOUPE. 2000. Compromised neural selectivity for song in birds with impaired sensorimotor learning. Neuron 25: 109-121
23. SOLIS, M.M. & A.J. DOUPE. 1997. Anterior forebrain neurons develop selectivity by an intermediate stage of birdsong learning. J. Neurosci. 17: 6447-6462.
24. SOLIS, M.M. & A.J. DOUPE. 1999. Contributions of tutor and bird's own song experience to neural selectivity in the songbird anterior forebrain. J. Neurosci. 19: 4559-4584.
25. DOUPE, A.J. 1997. Song- and order-selective neurons in the songbird anterior forebrain and their emergence during vocal development. J. Neurosci. 17: 1147-1167.
26. VOLMAN, S.F. 1993. Development of neural selectivity for birdsong during vocal learning. J. Neurosci. 13: 4737-4747.
27. KUHL, P.K. 1995. Learning and representation in speech and language. Curr. Opin. Neurobiol. 4: 812-822.
28. WERKER, J.F. & R.C. TEES. 1984. Phonemic and phonetic factors in adult cross-language speech perception. J. Acoust. Soc. Am. 75: 1866-1878.
29. HESSLER, N.A. & A.J. DOUPE. 1999. Social context modulates singing-related neural activity in the songbird forebrain. Nat. Neurosci. 2: 209-211.
30. HESSLER, N.A. & A.J. DOUPE. 1999. Singing-related neural activity in a dorsal forebrain-basal ganglia circuit of adult zebra finches. J. Neurosci. 19: 10461-10481.
31. BASHAM, M.E., E.J. NORDEEN & K.W. NORDEEN. 1996. Blockade of NMDA receptors in the anterior forebrain impairs sensory acquisition in the zebra finch. Neurobiol. Learning Mem. 66: 295-304.
32. SOLIS, M.M., M.S. BRAINARD, N.A. HESSLER & A.J. DOUPE. 2000. Song selectivity and sensorimotor signals in vocal learning and production. Proc. Natl. Acad. Sci. USA 97: 11836-11842.
33. MELLO, C.V., D.S. VICARIO & D.F. CLAYTON. 1992. Song presentation induces gene expression in the songbird forebrain. Proc. Natl. Acad. Sci. USA 89: 6818-6822.
34. BOLHUIS, J.J., G.G. ZIJLSTRA, A.M. DEN BOER-VISSER & E.A. VAN DER ZEE. 2000. Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc. Natl. Acad. Sci. USA 97: 2282-2285.
35. VICARIO, D.S. & K.H. YOHAY. 1993. Song-selective auditory input to a forebrain vocal control nucleus in the zebra finch. J. Neurobiol. 24: 488-505.
36. DAVE, A.S., A.C. YU & D. MARGOLIASH. 1998. Behavioral state modulation of auditory activity in a vocal motor system. Science 282: 2250-2254.
37. KIMPO, R.R., F.E. THEUNISSEN & A.J. DOUPE. 2003. Propagation of correlated activity through multiple stages of a neural circuit. J. Neurosci. 23: 5750-5761.
38. ROSENBERG, J.R., A.M. AMJAD, P. BREEZE, et al. 1989. The fourier approach to the identification of functional coupling between neuronal spike trains. Prog. Biophys. Molec. Biol. 53: 1-31.
39. BOTTJER, S.W., K.A. HALSEMA, S.A. BROWN & E.A. MIESNER, 1989. Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J. Comp. Neurol. 279: 312-326.
40. MOONEY, R. 1992. Synaptic basis for developmental plasticity in a birdsong nucleus. J. Neurosci. 12: 2464-2477.
41. VATES, G., D. VICARIO & F. NOTTEBOHM. 1997. Reafferent thalamo-"cortical" loops in the song system of oscine songbirds. J. Comp. Neurol. 380: 275-290.
42. FROSTIG, R.D., Y. GOTTLIEB, E. VAADIA & M. ABELES. 1983. The effects of stimuli on the activity and functional connectivity of local neuronal groups in cat auditory cortex. Brain Res. 272: 211-221.
43. GOCHIN, P.M., E.K. MILLER, C.G. GROSS & G.L. GERSTEIN. 1991. Functional interactions among neurons in inferior temporal cortex of the awake macaque. Exp. Brain Res. 84: 505-516.
44. MASON, A., A. NICOLL & K. STRATFORD. 1991. Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. J. Neurosci. 11: 72-84.
45. EGGERMONT, J.J. 1992. Neural interaction in cat primary auditory cortex. Dependence on recording depth, electrode separation, and age. J. Neurophysiol. 68: 1216-1228.
46. SHADLEN, M.N. & W.T. NEWSOME. 1998. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18: 3870-3896.
47. STEVENS, C.F. & A.M. ZADOR. 1998. Input synchrony and the irregular firing of cortical neurons. Nat. Neurosci. 1: 210-217.
48. CHOI, S. & D.M. LOVINGER. 1997. Decreased frequency but not amplitude of quantal synaptic responses associated with expression of corticostriatal long-term depression. J. Neurosci. 17: 8613-8620.
49. ABELES, M., E. VAADIA, H. BERGMAN, et al. 1993. Dynamics of neuronal interaction in the frontal cortex of behaving monkeys. Concepts Neurosci. 4: 131.
50. VAADIA, E., I. HAALMAN, M. ABELES, et al. 1995. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature 373: 515-518.
51. ALONSO, J. & L.M. MARTINEZ. 1998. Functional connectivity between simple cells and complex cells in cat striate cortex. Nat. Neurosci. 1: 395-403.
52. EGGERMONT, J.J. & G.M. SMITH. 1996. Neural connectivity only accounts for a small part of neural correlation in auditory cortex. Exp. Brain Res. 110: 379-391.
53. EIMAS, P.D., J.L. MILLER & P.W. JUSCZYK. 1987 On infant speech perception and language acquisition. In Categorical Perception. S. Harnard, Ed.: 161-195. Cambridge University Press. New York.
54. SUTTER M.L. & D. MARGOLIASH. 1994. Global synchronous response to autogenous song in zebra finch HVc. J. Neurophysiol. 72: 2105-2123.
55. HAHNLOSER, R.H., A.A. KOZHEVNIKOV & M.S. FEE. 2002. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419: 65-70.
56. FORTUNE, E.S. & D. MARGOLIASH. 1995. Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata). J. Comp. Neurol. 360: 413-441.
57. VATES, G.E. & F. NOTTEBOHM. 1995. Feedback circuitry within a song-learning pathway. Proc. Natl. Acad. Sci. USA 92: 5139-5143.
58. FOSTER, E.F. & S.W. BOTTJER. 1998. Axonal connections of the high vocal center and surrounding cortical regions in juvenile and adult male zebra finches. J. Comp. Neurol. 397: 118-138.
59. JOHNSON, F., M.M. SABLAN & S.W. BOTTJER. 1995. Topographic organization of a forebrain pathway involved with vocal learning in zebra finches. J. Comp. Neurol. 358: 260-278.
60. Luo, M., L. DING & D.J. PERKEL. 2001. An avian basal ganglia pathway essential for vocal learning forms a closed topographic loop. J. Neurosci. 21: 6836-6845.
61. BOETTIGER, C.A. & A.J. DOUPE. 2001. Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning. Neuron 31: 809-818.
62. SPIRO, J.E., M.B. DALVA & R. MOONEY. 1999. Long-range inhibition within the zebra finch song nucleus RA can coordinate the firing of multiple projection neurons. J. Neurophysiol. 81: 3007-3020.
63. CARDIN, J.A. & M.F. SCHMIDT. 2004. Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. J. Neurophysiol. (online preprint - "Articles in Press")
64. BOTTJER, S.W. 1993. The distribution of tyrosine hydroxylase immunoreactivity in the brains of male and female zebra finches. J. Neurobiol. 24: 51-69.
65. BOTTJER, S.W. & F. JOHNSON. 1997. Circuits, hormones, and learning: vocal behavior in songbirds. J. Neurobiol. 33: 602-618.
66. PERKEL, D.J. & M.A. FARRIES. 2000. Complementary "bottom- up" and "top-down" approaches to basal ganglia function. Curr. Opin. Neurobiol. 10: 725-731.
67. GRAYBIEL, A.M., T. AOSAKI, A.W. FLAHERTY & M. KIMURA. 1994. The basal ganglia and adaptive motor control. Science 265: 1826-1831.
68. GRAYBIEL, A.M. 1998. The basal ganglia and chunking of action repertoires. Neurobiol. Learn. Mem. 70: 119-136.
69. PARENT, A., F. SATO, Y. Wu, et al. 2000. Organization of the basal ganglia: the importance of axonal collateralization. Trends Neurosci. 23: S20-S27.
70. MIDDLETON, F.A. & P.L. STRICK. 2000. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res. Brain Res. Rev. 31: 236-250.
71. RAZ, A., A. FEINGOLD, V. ZELANSKAYA, et al. 1996. Neuronal synchronization of tonically active neurons in the striatum of normal and parkinsonian primates. J. Neurophysiol. 76: 2083-2088.
72. BERGMAN, H., A. FEINGOLD, A. NINI, et al. 1998. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. 21: 32-38.
73. BAR-GAD, I. & H. BERGMAN. 2001. Stepping out of the box: information processing in the neuronal networks of the basal ganglia. Curr. Opin. Neurobiol. 11: 689-695.
74. BEVAN, M.D., P.J. MAGILL, D. TERMAN, et al. 2002. Move to the rhythm: oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci. 25: 525-531.
75. STROEVE, S. & S. GIELEN. 2001. Correlation between uncoupled conductance-based integrate-and-fire neurons due to common and synchronous presynaptic firing. Neural Comput. 13: 2005-2029.
76. RUSKIN, D.N., D.A. BERGSTROM, Y. KANEOKE, et al. 1999. Multisecond oscillations in firing rate in the basal ganglia: robust modulation by dopamine receptor activation and anesthesia. J. Neurophysiol. 81: 2046-2055.
77. LEWIS, J.W., S.M. RYAN, A.P. ARNOLD & L.L. BUTCHER. 1981. Evidence for a catecholaminergic projection to area X in the zebra finch. J. Comp. Neurol. 196: 347-354.
78. SOHA, J.A., T. SHIMIZU & A.J. DOUPE. 1996. Development of the catecholaminergic innervation of the song system of the male zebra finch. J. Neurobiol. 29: 473-489.
79. APPELTANTS, D., P. ABSIL, J. BALTHAZART & G.F. BALL. 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: 117-33.
80. 3H]MK-801 binding within zebra finch song nuclei. J. Neurobiol. 23: 997-1005.
81. EALES, L.A. 1989. The influences of visual and vocal interaction on song learning in zebra finches. Anim. Behav. 37: 507-508.
82. BOETTIGER, C.A. & A.J. DOUPE. 1998. Intrinsic and thalamic excitatory inputs onto songbird LMAN neurons differ in their pharmacological and temporal properties. J. Neurophysiol. 79: 2615-2628.
83. LIVINGSTON, F.S. & R. MOONEY. 1997. Development of intrinsic and synaptic properties in a forebrain nucleus essential to avian song learning. J. Neurosci. 17: 8997-9009.
84. BOTTJER, S.W., J.D. BRADY & J.P. WALSH. 1998. Intrinsic and synaptic properties of neurons in the vocal-control nucleus IMAN from in vitro slice preparations of juvenile and adult zebra finches. J. Neurobiol. 37: 642-658.
85. ROBERTS, P.D. 1999. Computational consequences of temporally asymmetric learning rules: I. Differential Hebbian learning. J. Comput. Neurosci. 7: 235-246.
86. SONG, S., K.D. MILLER & L.F. ABBOTT. 2000. Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci. 3: 919-926.
87. BELL, C.C., V.Z. HAN, Y. SUGAWARA & K. GRANT. 1997. Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature 387: 278-281.
88. MAGEE, J.C. & D. JOHNSTON. 1997. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275: 209-213.
89. MARKRAM, H., J. LUBKE, M. FROTSCHER & B. SAKMANN. 1997. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275: 213-215.
90. BI, G.Q. & M.M. POO. 1998. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J. Neurosci. 18: 10464-10472.
91. DEBANNE, D., B.H. GAHWILER & S.M. THOMPSON. 1998. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J. Physiol. 507: 237-247.
92. ZHANG, L.I., H.W. TAO, C.E. HOLT, et al. 1998. A critical window for cooperation and competition among developing retinotectal synapses. Nature 395: 37-44.
93. EGGER, V., D. FELDMEYER & B. SAKMANN. 1999. Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nat. Neurosci. 2: 1098-1105.
94. FELDMAN, D.E. 2000. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27: 45-56.
95. HUA, S.E., J.C. HOUK & F.A. MUSSA-IVALDI. 1999. Emergence of symmetric, modular, and reciprocal connections in recurrent networks with Hebbian learning. Biol. Cybern. 81: 211-225.
96. EALES, L.A. 1987. Song learning in female-raised zebra finches: another look at the sensitive phase. Anim. Behav. 35: 1356-1365.
97. GERSTNER, W., R. RITZ & J.L. VAN HEMMEN. 1993. Why spikes? Hebbian learning and retrieval of time-resolved excitation patterns. Biol. Cybern. 69: 503-515.
98. ABBOTT, L.F. & K.I. BLUM. 1996. Functional significance of long-term potentiation for sequence learning and prediction. Cereb. Cortex 6: 406-416.
99. TROVER, T. & A.J. DOUPE. 2000. An association model of birdsong sensory motor learning I. Efference copy and the learning of song syllables. J. Neurophysiol. 84: 1204-1223
100. OJEMANN, G.A. 1991. Cortical organization of language. J. Neurosci. 11: 2281-2287.
101. CREUTZFELDT, O., G. OJEMANN & E. LETTICH. 1989. Neuronal activity in the human lateral temporal lobe. I. Responses to speech. Exp. Brain Res. 77: 451-475.
102. LUO, M. & D.J. PERKEL. 1999. Long-range GABAergic projection in a circuit essential for vocal learning. J. Comp. Neurol. 403: 68-84.
103. BERGMAN, H., A. FEINGOLD, A. NINI, et al. 1998. Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. 21: 32-38.
104. HIKOSAKA, O., M. SAKAMOTO & S. USUI. 1989. Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. J. Neurophysiol. 61: 814-832.
105. HOLLERMAN, J.R., L. TREMBLAY & W. SCHULTZ. 1998. Influence of reward expectation on behavior-related neuronal activity in primate striatum. J. Neurophysiol. 80: 947-963.
106. TREMBLAY, L., J.R. HOLLERMAN & W. SCHULTZ. 1998. Modifications of reward expectation-related neuronal activity during learning in primate striatum. J. Neurophysiol. 80: 964-977.
107. DIESMANN, M., M. GEWALTIG & A. AERTSEN. 1999. Stable propagation of synchronous spiking in cortical neural networks. Nature 402: 529-533
108. RAZ, A., V. FRECHTER-MAZAR, A. FEINGOLD, et al. 2001. Activity of pallidal and striatal tonically active neuron is correlated in MPTP-treated monkeys but not in normal monkeys. J. Neurosci. 21: 1-5.
109. DOUPE, A.J., M.M. SOLIS, C.A. BOETTIGER & N.A. HESSLER. 2004. Birdsong: hearing in the service of vocal learning. In The Cognitive Neurosciences III. M.S. Gazzaniga, Ed. MIT Press. Cambridge, MA.