Developmental regulation of basal ganglia circuitry during the sensitive period for vocal learning in songbirds

Annals of the New York Academy of Sciences

Volumn 1016, Issue , 2004, Pages 395-415

  Bottjer, Sarah W ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Axon pruning; Corollary discharge; NMDA receptor; Postsynaptic potentials; Sensorimotor integration; Silent synapses; Song system; Topography; Zebra finch

Indexed keywords

DIZOCILPINE; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ACOUSTICS; ATMOSPHERIC PRESSURE; AUDITORY CORTEX; BASAL GANGLION; BODY MOVEMENT; BRAIN REGION; CONFERENCE PAPER; DENDRITIC SPINE; FEEDBACK SYSTEM; FOREBRAIN; INTERPERSONAL COMMUNICATION; LEARNING; LIFESPAN; MOTOR ACTIVITY; MOTOR CORTEX; MOTOR PERFORMANCE; NERVE CELL; NERVE CELL NETWORK; NERVE FIBER; NEUROTRANSMITTER RELEASE; NONHUMAN; PHYSIOLOGY; RHOMBENCEPHALON; SINGING; SONGBIRD; THALAMUS; VOCALIZATION;

ANIMALIA; AVES; PASSERI; TAENIOPYGIA GUTTATA;

EID: 3242704882     PISSN: 00778923     EISSN: None     Source Type: Book Series    
DOI: 10.1196/annals.1298.037     Document Type: Conference Paper

References (96)

1. MARLER, P. 1970. A comparative approach to vocal learning: song development in white-crowned sparrows. J. Comp. Physiol. Psychol. 71: 1-25.
2. MARLER, P. & S. PETERS. 1981. Sparrow learn adult song and more from memory. Science 213: 780-782.
3. MARLER, P. & S. PETERS. 1982. Long-term storage of learned birdsongs prior to production. Anim. Behav. 30: 479-482.
4. KONISHI, M. 1965. Effects of deafening on song development in American robins and black-headed grosbeaks. Z. Tierpsychol. 22: 584-599.
5. MARLER, P. 1997. Three models of song learning: evidence from behavior. J. Neurobiol. 33: 501-516.
6. 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.
7. FUNABIKI, Y. & M. KONISHI. 2003. Long memory in song learning by zebra finches. J. Neurosci. 23: 6928-6935.
8. TCHERNICHOVSKI, O., P.P. MITRA, T. LINTS & F. NOTTEBOHM. 2001. Dynamics of the vocal imitation process: how a zebra finch learns its song. Science 291: 2564-2569.
9. KONISHI, M. & E. AKUTAGAWA. 1985. Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature 315: 145-147.
10. NORDEEN, K.W. & E.J. NORDEEN. 1988. Projection neurons within a vocal motor pathway are born during song learning in zebra finches. Nature 334: 149-151.
11. NOTTEBOHM, F., T.M. STOKES & C.M. LEONARD. 1976. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165: 457-486.
12. VU, E.T., M.E. MAZUREK & Y.C. KUO. 1994. Identification of a forebrain motor programming network for the learned song of zebra finches. J. Neurosci. 14: 6924-6934.
13. YU, A.C. & D. MARGOLIASH. 1996. Temporal hierarchical control of singing in birds [see comments]. Science 273: 1871-1875.
14. 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.
15. 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.
16. 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.
17. 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.
18. VOLMAN, S.F. 1993. Development of neural selectivity for birdsong during vocal learning. J. Neurosci. 13: 4737-4747.
19. SOLIS, M.M. & A.J. DOUPE. 1997. Anterior forebrain neurons develop selectivity by an intermediate stage of birdsong learning. J. Neurosci. 17: 6447-6462.
20. RAUSKE, P.L., S.D. SHEA & D. MARGOLIASH. 2003. State and neuronal class-dependent reconfiguration in the avian song system. J. Neurophysiol. 89: 1688-1701.
21. CARDIN, J.A. & M.F. SCHMIDT. 2003. Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. J. Neurophysiol. 90: 2884-2899.
22. SOLIS, M.M. & A.J. DOUPE. 2000. Compromised neural selectivity for song in birds with impaired sensorimotor learning. Neuron 25: 109-121.
23. ALVAREZ-BUYLLA, A., M. THEELEN & F. NOTTEBOHM. 1988. Birth of projection neurons in the higher vocal center of the canary forebrain before, during, and after song learning. Proc. Natl. Acad. Sci. USA 85: 8722-8726.
24. MOONEY, R. & M. RAO. 1994. Waiting periods versus early innervation: the development of axonal connections in the zebra finch song system. J. Neurosci. 14: 6532-6543.
25. FARRIES, M.A. & D.J. PERKEL. 2002. A telencephalic nucleus essential for song learn-ing contains neurons with physiological characteristics of both striatum and globus pallidus. J. Neurosci. 22: 3776-3787.
26. REINER, A., A.V. LAVERGHETTA, C.A. MEADE, et al. 2004. An immunohistochemical and pathway tracing study of the striatopallidal organization of area X in the male zebra finch. J. Comp. Neurol. 469: 239-261.
27. BOTTJER, S.W. & A.P. ARNOLD. 1984. The role of feedback from the vocal organ. I. Maintenance of stereotypical vocalizations by adult zebra finches. J. Neurosci. 4: 2387-2396.
28. 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.
29. BOTTJER, S.W. & A.P. ARNOLD. 1986. Handbook of Behavioral Neurobiology: Dev. Proc. Psychobiol. Neurobiol: 129-161.
30. JOHNSON, F. & S.W. BOTTJER. 1992. Growth and regression of thalamic efferents in the song-control system of male zebra finches. J. Comp. Neurol. 326: 442-450.
31. 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.
32. BOTTJER, S.W., J.D. BRADY & B. CRIBBS. 2000. Connections of a motor cortical region in zebra finches: relation to pathways for vocal learning. J. Comp. Neurol. 420: 244-260.
33. FOSTER, E.F., R.P. MEHTA & S.W. BOTTJER. 1997. Axonal connections of the medial magnocellular nucleus of the anterior neostriatum in zebra finches. J. Comp. Neurol. 382: 364-381.
34. VATES, G.E. & F. NOTTEBOHM. 1995. Feedback circuitry within a song-learning pathway. Proc. Natl. Acad. Sci. USA 92: 5139-5143.
35. VATES, G.E., D.S. VICARIO & F. NOTTEBOHM. 1997. Reafferent thalamo-"cortical" loops in the song system of oscine songbirds. J. Comp. Neurol. 380: 275-290.
36. IYENGAR, S., S.S. VISWANATHAN & S.W. BOTTJER. 1999. Development of topography within song control circuitry of zebra finches during the sensitive period for song learning. J. Neurosci. 19: 6037-6057.
37. WILD, J.M. 1997. Neural pathways for the control of birdsong production. J. Neurobiol. 33: 653-670.
38. VICARIO, D.S. 1991. Neural mechanisms of vocal production in songbirds. Curr. Opin. Neurobiol. 1: 595-600.
39. WILD, J.M. 1993. Descending projections of the songbird nucleus robustus archistriatalis. J. Comp. Neurol. 338: 225-241.
40. LUO, M. & D.J. PERKEL. 1999. A GABAergic, strongly inhibitory projection to a thalamic nucleus in the zebra finch song system. J. Neurosci. 19: 6700-6711.
41. MOONEY, R., M.J. ROSEN & C.B. STURDY. 2002. A bird's eye view: top down intracellular analyses of auditory selectivity for learned vocalizations. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 188: 879-895.
42. 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.
43. NORDEEN, K.W. & E.J. NORDEEN. 1993. Long-term maintenance of song in adult zebra finches is not affected by lesions of a forebrain region involved in song learning. Behav. Neural Biol. 59: 79-82.
44. 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.
45. KORSIA, S. & S.W. BOTTJER. 1989. Developmental changes in the cellular composition of a brain nucleus involved with song learning in zebra finches. Neuron 3: 451-460.
46. BOTTJER, S.W., H. ROSELINSKY & N.B. TRAN. 1997. Sex differences in neuropeptide staining of song-control nuclei in zebra finch brains. Brain Behav. Evol. 50: 284-303.
47. 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.
48. ROSEN, M.J. & R. MOONEY. 2000. Intrinsic and extrinsic contributions to auditory selectivity in a song nucleus critical for vocal plasticity. J. Neurosci. 20: 5437-5448.
49. BRAINARD, M.S. & A.J. DOUPE. 2000. Auditory feedback in learning and maintenance of vocal behaviour. Nat. Rev. Neurosci. 1: 31-40.
50. TROYER, T.W. & S.W. BOTTJER. 2001. Birdsong: models and mechanisms. Curr. Opin. Neurobiol. 11: 721-726.
51. GUILLERY, R.W. & S.M. SHERMAN. 2002. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33: 163-175.
52. FOSTER, E.F. & S.W. BOTTJER. 2001. Lesions of a telencephalic nucleus in male zebra finches: influences on vocal behavior in juveniles and adults. J. Neurobiol. 46: 142-165.
53. BRAINARD, M.S. & A.J. DOUPE. 2000. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404: 762-766.
54. WILLIAMS, H. & F. NOTTEBOHM. 1985. Auditory responses in avian vocal motor neurons: a motor theory for song perception in birds. Science 229: 279-282.
55. PEARSON, K. 2000. Motor systems. Curr. Opin. Neurobiol. 10: 649-654.
56. PRICE, P.H. 1979. Developmental determinants of structure in zebra finch song. J. Comp. Physiol. Psychol. 93: 260-277.
57. OKANOYA, K. & A. YAMAGUCHI. 1997. Adult Bengalese finches (Lonchura striata var. domestica) require real-time auditory feedback to produce normal song syntax. J. Neurobiol. 33: 343-356.
58. WOOLLEY, S.M. & E.W. RUBEL. 1997. Bengalese finches Lonchura striata domestica depend upon auditory feedback for the maintenance of adult song. J. Neurosci. 17: 6380-6390.
59. 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.
60. LEONARDO, A. & M. KONISHI. 1999. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399: 466-470.
61. LOMBARDINO, A.J. & F. NOTTEBOHM. 2000. Age at deafening affects the stability of learned song in adult male zebra finches. J. Neurosci. 20: 5054-5064.
62. ZEVIN, J.D., M.S. SEIDENBER & S.W. BOTTJER. 2004. Limits on reacquisition of song learning in adult zebra finches exposed to white noise. J. Neurosci. In press.
63. SUTHERS, R.A., F. GOLLER & J.M. WILD. 2002. Somatosensory feedback modulates the respiratory motor program of crystallized birdsong. Proc. Natl. Acad. Sci. USA 99: 5680-5685.
64. WOOLLEY, S.M. & E.W. RUBEL. 2002. Vocal memory and learning in adult Bengalese finches with regenerated hair cells. J. Neurosci. 22: 7774-7787.
65. BRAINARD, M.S. & A.J. DOUPE. 2001. Postlearning consolidation of birdsong: stabilizing effects of age and anterior forebrain lesions. J. Neurosci. 21: 2501-2517.
66. IYENGAR, S. & S.W. BOTTJER. 2002. Development of individual axon arbors in a thalamo-cortical circuit necessary for song learning in zebra finches. J. Neurosci. 22: 901-911.
67. NIXDORF-BERGWEILER, B.E. 2001. Lateral magnocellular nucleus of the anterior neostriatum (LMAN) in the zebra finch: neuronal connectivity and the emergence of sex differences in cell morphology. Microsc. Res. Tech. 54: 335-353.
68. NOTTEBOHM, F., S. KASPARIAN & C. PANDAZIS. 981. Brain space for a learned task. Brain Res. 213: 99-109.
69. WEINBERGER, N.M. 1995. Dynamic regulation of receptive fields and maps in the adult sensory cortex. Annu. Rev. Neurosci. 18: 129-158.
70. NIXDORF-BERGWEILER, B.E., E. WALLHAUSSER-FRANKE & T.J. DEVOOGD. 1995. Regressive development in neuronal structure during song learning in birds. J. Neurobiol. 27: 204-215.
71. IYENGAR, S. & S.W. BOTTJER. 2002. The role of auditory experience in the formation of neural circuits underlying vocal learning in zebra finches. J. Neurosci. 22: 946-958.
72. DAVE, A.S. & D. MARGOLIASH. 2000. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290: 812-816.
73. AAMODT, S.M., E.J. NORDEEN & K.W. NORDEEN. 1995. Early isolation from conspecific song does not affect the normal developmental decline of N-methyl-D-aspartate receptor binding in an avian song nucleus. J. Neurobiol. 27: 76-84.
74. BASHAM, M.E., F. SOHRABJI, T.D. SINGH, et al. 1999. Developmental regulation of NMDA receptor 2B subunit mRNA and ifenprodil binding in the zebra finch anterior forebrain. J. Neurobiol. 39: 155-167.
75. 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.
76. WHITE, S.A., F.S. LIVINGSTON & R. MOONEY. 1999. Androgens modulate NMDA receptor-mediated EPSCs in the zebra finch song system. J. Neurophysiol. 82: 2221-2234.
77. LIVINGSTON, F.S., S.A. WHITE & R. MOONEY. 2000. Slow NMDA-EPSCs at synapses critical for song development are not required for song learning in zebra finches. Nat. Neurosci. 3: 482-488.
78. SINGH, T.D., M.E. BASHAM, E.J. NORDEEN & K.W. NORDEEN. 2000. Early sensory and hormonal experience modulate age-related changes in NR2B mRNA within a forebrain region controlling avian vocal learning. J. Neurobiol. 44: 82-94.
79. ROBERTS, E.B. & A.S. RAMOA. 1999. Enhanced NR2A subunit expression and decreased NMDA receptor decay time at the onset of ocular dominance plasticity in the ferret. J. Neurophysiol. 81: 2587-2591.
80. KORSIA, S. & S.W. BOTTJER. 1991. Chronic testosterone treatment impairs vocal learning in male zebra finches during a restricted period of development. J. Neurosci. 11: 2362-2371.
81. GRAMMER, M.K. & S.W. BOTTJER. 2001. Silent synapses at neural substrates important for song learning in zebra finches. Soc. Neurosci. Abstr. 27: 1424.
82. LIAO, D., N.A. HESSLER & R. MALINOW. 1995. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375: 400-404.
83. ISAAC, J.T., R.A. NICOLL & R.C. MALENKA. 1995. Evidence for silent synapses: implications for the expression of LTP. Neuron 15: 427-434.
84. DURAND, G.M., Y. KOVALCHUK & A. KONNERTH. 1996. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381: 71-75.
85. WU, G., R. MALINOW & H.T. CLINE. 1996. Maturation of a central glutamatergic synapse. Science 274: 972-976.
86. STARK, L.L. & D.J. PERKEL. 1999. Two-stage, input-specific synaptic maturation in a nucleus essential for vocal production in the zebra finch. J. Neurosci. 19: 9107-9116.
87. BOETTIGER, C.A. & A.J. DOUPE. 2001. Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning. Neuron 31: 809-818.
88. DING, L. & D.J. PERKEL. 2004. Long-term potentiation in an avian basal ganglia nucleus essential for vocal learning. J. Neurosci. 24: 488-494.
89. BOTTJER, S.W. 2002. Neural strategies for learning during sensitive periods of development. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 188: 917-928.
90. FELDMAN, D.E., M.S. BRAINARD & E.I. KNUDSEN. 1996. Newly learned auditory responses mediated by NMDA receptors in the owl inferior colliculus. Science 271: 525-528.
91. 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.
92. SUTHERS, R.A. & D. MARGOLIASH. 2002. Motor control of birdsong. Curr. Opin. Neurobiol. 12: 684-690.
93. CHI, Z. & D. MARGOLIASH. 2001. Temporal precision and temporal drift in brain and behavior of zebra finch song. Neuron 32: 899-910.
94. KITTELBERGER, J.M. & R. MOONEY. 1999. Lesions of an avian forebrain nucleus that disrupt song development alter synaptic connectivity and transmission in the vocal premotor pathway. J. Neurosci. 19: 9385-9398.
95. MOONEY, R. 1992. Synaptic basis for developmental plasticity in a birdsong nucleus. J. Neurosci. 12: 2464-2477.
96. HERRMANN, K. & A.P. ARNOLD. 1991. The development of afferent projections to the robust archistriatal nucleus in male zebra finches: a quantitative electron microscopic study. J. Neurosci. 11: 2063-2074.