Neuron-specific cholinergic modulation of a forebrain song control nucleus

Journal of Neurophysiology

Volumn 103, Issue 2, 2010, Pages 733-745

  Shea, Stephen D ^a   Koch, Henner ^b   Baleckaitis, Daniel ^b   Ramirez, Jan Marino ^a,b   Margoliash, Daniel ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ATROPINE; CHOLINERGIC RECEPTOR STIMULATING AGENT; MUSCARINIC RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASAL GANGLION; BRAIN CELL; BRAIN ELECTROPHYSIOLOGY; CELL SPECIFICITY; CHOLINERGIC ACTIVITY; FOREBRAIN; IN VITRO STUDY; INTERNEURON; MALE; MEMBRANE STEADY POTENTIAL; MOTONEURON NUCLEUS; MUSIC; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SINGING; SPIKE WAVE; SYNAPTIC TRANSMISSION; WHOLE CELL;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; CHOLINERGIC FIBERS; FINCHES; MALE; NERVE NET; NEURONAL PLASTICITY; NEURONS; PROSENCEPHALON; VOCALIZATION, ANIMAL;

EID: 76649110524     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00803.2009     Document Type: Article

References (76)

1. Aghajanian GK, Rasmussen K. Intracellular studies in the facial nucleus illustrating a simple new method for obtaining viable motoneurons in adult rat brain slices. Synapse 3: 331-338, 1989.
2. Akutagawa E, Konishi M. Connections of thalamic modulatory centers to the vocal control system of the zebra finch. Proc Natl Acad Sci USA 102: 14086-14091, 2005.
3. Alvarez-Buylla A, Kirn JR, Nottebohm F. Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 249: 1444-1446, 1990.
4. Ball GF, Nock B, Wingfield JC, McEwen BS, Balthazart J. Muscarinic cholinergic receptors in the songbird and quail brain: a quantitative autoradiographic study. J Comp Neurol 298: 431-442, 1990.
5. Bauer EE, Coleman MJ, Roberts TF, Roy A, Prather JF, Mooney R. A synaptic basis for auditory-vocal integration in the songbird. J Neurosci 28: 1509-1522, 2008.
6. Benton S, Cardin JA, DeVoogd TJ. Lucifer Yellow filling of Area X projecting neurons in the high vocal center of female canaries. Brain Res 799: 138-147, 1998.
7. Bottjer SW, Miesner EA, Arnold AP. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224: 901-903, 1984.
8. Brainard MS, Doupe AJ. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404: 762-766, 2000.
9. Brenowitz EA. Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science 251: 303-305, 1991.
10. Burt JM, Lent KL, Beecher MD, Brenowitz EA. Lesions of the anterior forebrain song control pathway in female canaries affect song perception in an operant task. J Neurobiol 42: 1-13, 2000.
11. Cardin JA, Schmidt MF. Song system auditory responses are stable and highly tuned during sedation, rapidly modulated and unselective during wakefulness, and suppressed by arousal. J Neurophysiol 90: 2884-2899, 2003.
12. Cardin JA, Schmidt MF. Noradrenergic inputs mediate state dependence of auditory responses in the avian song system. J Neurosci 24: 7745-7753, 2004.
13. Coleman MJ, Mooney R. Synaptic transformations underlying highly selective auditory representations of learned birdsong. J Neurosci 24: 7251-7265, 2004.
14. Coleman MJ, Mooney R. Thalamic gating of auditory responses in telencephalic song control nuclei. J Neurosci 27: 10024-10036, 2007.
15. Dave AS, Margoliash D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290: 812-816, 2000.
16. Dave AS, Yu AC, Margoliash D. Behavioral state modulation of auditory activity in a vocal motor system. Science 282: 2250-2254, 1998.
17. AHP in reticularis neurons. J Neurophysiol 79: 2911-2918, 1998.
18. Doupe AJ, Konishi M. Song-selective auditory circuits in the vocal control system of the zebra finch. Proc Natl Acad Sci USA 88: 11339-11343, 1991.
19. Dutar P, Petrozzino JJ, Vu HM, Schmidt MF, Perkel DJ. Slow synaptic inhibition mediated by metabotropic glutamate receptor activation of GIRK channels. J Neurophysiol 84: 2284-2290, 2000.
20. Dutar P, Vu HM, Perkel DJ. Multiple cell types distinguished by physiological, pharmacological, and anatomic properties in nucleus HVc of the adult zebra finch. J Neurophysiol 80: 1828-1838, 1998.
21. Fanselow EE, Richardson KA, Connors BW. Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100: 2640-2652, 2008.
22. Farries MA, Perkel DJ. A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus. J Neurosci 22: 3776-3787, 2002.
23. Fiete IR, Hahnloser RH, Fee MS, Seung HS. Temporal sparseness of the premotor drive is important for rapid learning in a neural network model of birdsong. J Neurophysiol 92: 2274-2282, 2004.
24. Fortune ES, Margoliash D. Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches (Taeniopygia guttata). J Comp Neurol 360: 413-441, 1995.
25. Gentner TQ, Hulse SH, Bentley GE, Ball GF. Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds. J Neurobiol 42: 117-133, 2000.
26. Gil Z, Connors BW, Amitai Y. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron 19: 679-686, 1997.
27. Gulledge AT, Stuart GJ. Cholinergic inhibition of neocortical pyramidal neurons. J Neurosci 25: 10308-10320, 2005.
28. Hahnloser RH, Kozhevnikov AA, Fee MS. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419: 65-70, 2002.
29. Haj-Dahmane S, Andrade R. Muscarinic activation of a voltage-dependent cation nonselective current in rat association cortex. J Neurosci 16: 3848-3861, 1996.
30. 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.
31. Hartigan JA, Hartigan PM. The dip test of unimodality. Annals Stat 13: 70-84, 1985.
32. Hsieh CY, Cruikshank SJ, Metherate R. Differential modulation of auditory thalamocortical and intracortical synaptic transmission by cholinergic agonist. Brain Res 880: 51-64, 2000.
33. Janata P, Margoliash D. Gradual emergence of song selectivity in sensorimotor structures of the male zebra finch song system. J Neurosci 19: 5108-5118, 1999.
34. + currents. Neurosci Lett 231: 13-16, 1997.
35. 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.
36. Kawaguchi Y. Selective cholinergic modulation of cortical GABAergic cell subtypes. J Neurophysiol 78: 1743-1747, 1997.
37. Kimpo RR, Theunissen FE, Doupe AJ. Propagation of correlated activity through multiple stages of a neural circuit. J Neurosci 23: 5750-5761, 2003.
38. Kirn JR, Alvarez-Buylla A, Nottebohm F. Production and survival of projection neurons in a forebrain vocal center of adult male canaries. J Neurosci 11: 1756-1762, 1991.
39. Kozhevnikov AA, Fee MS. Singing-related activity of identified HVC neurons in the zebra finch. J Neurophysiol 97: 4271-4283, 2007.
40. Kubota M, Taniguchi I. Electrophysiological characteristics of classes of neuron in the HVc of the zebra finch. J Neurophysiol 80: 914-923, 1998.
41. Leonardo A, Fee MS. Ensemble coding of vocal control in birdsong. J Neurosci 25: 652-661, 2005.
42. 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.
43. 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.
44. Lucas-Meunier E, Monier C, Amar M, Baux G, Fregnac Y, Fossier P. Involvement of nicotinic and muscarinic receptors in the endogenous cholinergic modulation of the balance between excitation and inhibition in the young rat visual cortex. Cereb Cortex 19: 2411-2427, 2009.
45. McCormick DA, Prince DA. Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol 375: 169-194, 1986.
46. Mooney R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J Neurosci 20: 5420-5436, 2000.
47. Mooney R, Prather JF. The HVC microcircuit: the synaptic basis for interactions between song motor and vocal plasticity pathways. J Neurosci 25: 1952-1964, 2005.
48. Nick TA, Konishi M. Neural song preference during vocal learning in the zebra finch depends on age and state. J Neurobiol 62: 231-242, 2005.
49. Nixdorf BE, Davis SS, DeVoogd TJ. Morphology of Golgi-impregnated neurons in hyperstriatum ventralis, pars caudalis in adult male and female canaries. J Comp Neurol 284: 337-349, 1989.
50. Nottebohm F, Stokes TM, Leonard CM. Central control of song in the canary, Serinus canarius. J Comp Neurol 165: 457-486, 1976.
51. ölveczky BP, Andalman AS, Fee MS. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol 3: 902-909, 2005.
52. Prather JF, Nowicki S, Anderson RC, Peters S, Mooney R. Neural correlates of categorical perception in learned vocal communication. Nat Neurosci 12: 221-228, 2009.
53. Prather JF, Peters S, Nowicki S, Mooney R. Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 451: 305-310, 2008.
54. Rauske PL, Shea SD, Margoliash D. State and neuronal class-dependent reconfiguration in the avian song system. J Neurophysiol 89: 1688-1701, 2003.
55. 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, Güntürkün 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, of the Avian Brain Nomenclature Forum. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473: 377-414, 2004.
56. Rosen MJ, Mooney R. Inhibitory and excitatory mechanisms underlying auditory responses to learned vocalizations in the songbird nucleus HVC. Neuron 39: 177-194, 2003.
57. Rosen MJ, Mooney R. Synaptic interactions underlying song-selectivity in the avian nucleus HVC revealed by dual intracellular recordings. J Neurophysiol 95: 1158-1175, 2006.
58. Ryan SM, Arnold AP. Evidence for cholinergic participation in the control of birdsong: acetylcholinesterase distribution and muscarinic receptor autoradiography in the zebra finch brain. J Comp Neurol 202: 211-219, 1981.
59. Sakaguchi H, Saito N. Developmental change of cholinergic activity in the forebrain of the zebra finch during song learning. Brain Res Dev Brain Res 62: 223-228, 1991.
60. Sanchez-Vives MV, McCormick DA. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027-1034, 2000.
61. Scharff C, Nottebohm F. 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, 1991.
62. Scharff C, Nottebohm F, Cynx J. Conspecific and heterospecific song discrimination in male zebra finches with lesions in the anterior forebrain pathway. J Neurobiol 36: 81-90, 1998.
63. Schmidt MF, Konishi M. Gating of auditory responses in the vocal control system of awake songbirds. Nat Neurosci 1: 513-518, 1998.
64. Schmidt MF, Perkel DJ. Slow synaptic inhibition in nucleus HVc of the adult zebra finch. J Neurosci 18: 895-904, 1998.
65. Scott BB, Lois C. Developmental origin and identity of song system neurons born during vocal learning in songbirds. J Comp Neurol 502: 202-214, 2007.
66. Shank SS, Margoliash D. Sleep and sensorimotor integration during early vocal learning in a songbird. Nature 458: 73-77, 2009.
67. Shea SD, Margoliash D. Basal forebrain cholinergic modulation of auditory activity in the zebra finch song system. Neuron 40: 1213-1226, 2003.
68. Sohrabji F, Nordeen EJ, Nordeen KW. Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behav Neural Biol 53: 51-63, 1990.
69. 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, 2000a.
70. Troyer TW, Doupe AJ. An associational model of birdsong sensorimotor learning. II. Temporal hierarchies and the learning of song sequence. J Neurophysiol 84: 1224-1239, 2000b.
71. Tryba AK, Peña F, Lieske SP, Viemari JC, Thoby-Brisson M, Ramirez JM. Differential modulation of neural network and pacemaker activity underlying eupnea and sigh-breathing activities. J Neurophysiol 99: 2114-2125, 2008.
72. Vicario DS, Yohay KH. Song-selective auditory input to a forebrain vocal control nucleus in the zebra finch. J Neurobiol 24: 488-505, 1993.
73. Wild JM, Williams MN, Howie GJ, Mooney R. Calcium-binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata). J Comp Neurol 483: 76-90, 2005.
74. Williams H, Mehta N. Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production. J Neurobiol 39: 14-28, 1999.
75. Xiang Z, Huguenard JR, Prince DA. Cholinergic switching within neocortical inhibitory networks. Science 281: 985-988, 1998.
76. Xiao Z, Deng PY, Yang C, Lei S. Modulation of GABAergic transmission by muscarinic receptors in the entorhinal cortex of juvenile rats. J Neurophysiol 102: 659-669, 2009.