Deafening Drives Cell-Type-Specific Changes to Dendritic Spines in a Sensorimotor Nucleus Important to Learned Vocalizations

Neuron

Volumn 73, Issue 5, 2012, Pages 1028-1039

  Tschida, Katherine A ^a   Mooney, Richard ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY FEEDBACK; CELL SPECIFICITY; CONTROLLED STUDY; DENDRITIC SPINE; FINCH; HEARING IMPAIRMENT; IN VIVO STUDY; MALE; NERVE CELL EXCITABILITY; NERVE POTENTIAL; NERVE TRACT; NONHUMAN; PRIORITY JOURNAL; SENSORIMOTOR CORTEX; STRIATOTHALAMIC PATHWAY; SYNAPSE; VOCALIZATION;

AGE FACTORS; ANIMALS; AUDITORY PATHWAYS; BIOFEEDBACK, PSYCHOLOGY; DEAFNESS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; FINCHES; GREEN FLUORESCENT PROTEINS; HIGH VOCAL CENTER; LEARNING; LONGITUDINAL STUDIES; MALE; SENSORY RECEPTOR CELLS; SOUND SPECTROGRAPHY; SYNAPTIC TRANSMISSION; TIME FACTORS; VOCALIZATION, ANIMAL;

EID: 84858028380     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.12.038     Document Type: Article

References (67)

1. Alvarez V.A., Sabatini B.L. Anatomical and physiological plasticity of dendritic spines. Annu. Rev. Neurosci. 2007, 30:79-97.
2. Andalman A.S., Fee M.S. A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors. Proc. Natl. Acad. Sci. USA 2009, 106:12518-12523.
3. Bauer E.E., Coleman M.J., Roberts T.F., Roy A., Prather J.F., Mooney R. A synaptic basis for auditory-vocal integration in the songbird. J. Neurosci. 2008, 28:1509-1522.
4. Brainard M.S., Doupe A.J. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 2000, 404:762-766.
5. Cardin J.A., Schmidt M.F. Auditory responses in multiple sensorimotor song system nuclei are co-modulated by behavioral state. J. Neurophysiol. 2004, 91:2148-2163.
6. Cardin J.A., Raksin J.N., Schmidt M.F. Sensorimotor nucleus NIf is necessary for auditory processing but not vocal motor output in the avian song system. J. Neurophysiol. 2005, 93:2157-2166.
7. Coleman M.J., Mooney R. Synaptic transformations underlying highly selective auditory representations of learned birdsong. J. Neurosci. 2004, 24:7251-7265.
8. Damasio A.R., Damasio H., Rizzo M., Varney N., Gersh F. Aphasia with nonhemorrhagic lesions in the basal ganglia and internal capsule. Arch. Neurol. 1982, 39:15-24.
9. De Robertis E.D.P., Bennett H.S. Some features of the submicroscopic morphology of synapses in frog and earthworm. J. Biophys. Biochem. Cytol. 1955, 1:47-58.
10. De Roo M., Klauser P., Muller D. LTP promotes a selective long-term stabilization and clustering of dendritic spines. PLoS Biol. 2008, 6:e219.
11. Eliades S.J., Wang X. Sensory-motor interaction in the primate auditory cortex during self-initiated vocalizations. J. Neurophysiol. 2003, 89:2194-2207.
12. Eliades S.J., Wang X. Dynamics of auditory-vocal interaction in monkey auditory cortex. Cereb. Cortex 2005, 15:1510-1523.
13. Eliades S.J., Wang X. Neural substrates of vocalization feedback monitoring in primate auditory cortex. Nature 2008, 453:1102-1106.
14. Emmorey K., Allen J.S., Bruss J., Schenker N., Damasio H. A morphometric analysis of auditory brain regions in congenitally deaf adults. Proc. Natl. Acad. Sci. USA 2003, 100:10049-10054.
15. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399:66-70.
16. Fujimoto H., Hasegawa T., Watanabe D. Neural coding of syntactic structure in learned vocalizations in the songbird. J. Neurosci. 2011, 31:10023-10033.
17. Hahnloser R.H., Kozhevnikov A.A., Fee M.S. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 2002, 419:65-70.
18. Hofer S.B., Mrsic-Flogel T.D., Bonhoeffer T., Hübener M. Experience leaves a lasting structural trace in cortical circuits. Nature 2009, 457:313-317.
19. Holtmaat A., Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 2009, 10:647-658.
20. Holtmaat A., Wilbrecht L., Knott G.W., Welker E., Svoboda K. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 2006, 441:979-983.
21. Horita H., Wada K., Jarvis E.D. Early onset of deafening-induced song deterioration and differential requirements of the pallial-basal ganglia vocal pathway. Eur. J. Neurosci. 2008, 28:2519-2532.
22. Keck T., Mrsic-Flogel T.D., Vaz Afonso M., Eysel U.T., Bonhoeffer T., Hübener M. Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nat. Neurosci. 2008, 11:1162-1167.
23. Keck T., Scheuss V., Jacobsen R.I., Wierenga C.J., Eysel U.T., Bonhoeffer T., Hübener M. Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 2011, 71:869-882.
24. Keller G.B., Hahnloser R.H. Neural processing of auditory feedback during vocal practice in a songbird. Nature 2009, 457:187-190.
25. Kim D.J., Park S.Y., Kim J., Lee D.H., Park H.J. Alterations of white matter diffusion anisotropy in early deafness. Neuroreport 2009, 20:1032-1036.
26. Konishi M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 1965, 22:770-783.
27. Kopec C.D., Li B., Wei W., Boehm J., Malinow R. Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J. Neurosci. 2006, 26:2000-2009.
28. Kotak V.C., Fujisawa S., Lee F.A., Karthikeyan O., Aoki C., Sanes D.H. Hearing loss raises excitability in the auditory cortex. J. Neurosci. 2005, 25:3908-3918.
29. Kotak V.C., Takesian A.E., Sanes D.H. Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex. Cereb. Cortex 2008, 18:2098-2108.
30. Kozhevnikov A.A., Fee M.S. Singing-related activity of identified HVC neurons in the zebra finch. J. Neurophysiol. 2007, 97:4271-4283.
31. Lei H., Mooney R. Manipulation of a central auditory representation shapes learned vocal output. Neuron 2010, 65:122-134.
32. Leonardo A., Konishi M. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 1999, 399:466-470.
33. Lombardino A.J., Nottebohm F. Age at deafening affects the stability of learned song in adult male zebra finches. J. Neurosci. 2000, 20:5054-5064.
34. Maletic-Savatic M., Malinow R., Svoboda K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 1999, 283:1923-1927.
35. Marik S.A., Yamahachi H., McManus J.N., Szabo G., Gilbert C.D. Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLoS Biol. 2010, 8:e1000395.
36. Marler P. A comparative approach to vocal learning: song development in white-crowned sparrows. J. Comp. Physiol. Psychol. 1970, 71:1-25.
37. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
38. Mooney R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J. Neurosci. 2000, 20:5420-5436.
39. Mooney R., Prather J.F. The HVC microcircuit: the synaptic basis for interactions between song motor and vocal plasticity pathways. J. Neurosci. 2005, 25:1952-1964.
40. Nägerl U.V., Eberhorn N., Cambridge S.B., Bonhoeffer T. Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 2004, 44:759-767.
41. Nordeen K.W., Nordeen E.J. Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav. Neural Biol. 1992, 57:58-66.
42. Noreña A.J., Eggermont J.J. Changes in spontaneous neural activity immediately after an acoustic trauma: implications for neural correlates of tinnitus. Hear. Res. 2003, 183:137-153.
43. Nottebohm F., Stokes T.M., Leonard C.M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 1976, 165:457-486.
44. Okamoto K., Nagai T., Miyawaki A., Hayashi Y. Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 2004, 7:1104-1112.
45. Palay S.L. Synapses in the central nervous system. J. Biophys. Biochem. Cytol. 1956, 2(4 Suppl):193-202.
46. Petitto L.A. On the ontogenetic requirements for early language acquisition. Developmental Neurocognition: Speech and Face Processing in the First Year of Life 1993, 365-383. Kluwer, Dordrecht, Netherlands. B. de Boysson-Bardies, S. de Schonen, P. Jusczyk, P. MacNeilage, J. Morton (Eds.).
47. Prather J.F., Peters S., Nowicki S., Mooney R. Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 2008, 451:305-310.
48. Roberts T.F., Tschida K.A., Klein M.E., Mooney R. Rapid spine stabilization and synaptic enhancement at the onset of behavioural learning. Nature 2010, 463:948-952.
49. Roy A., Mooney R. Song decrystallization in adult zebra finches does not require the song nucleus NIf. J. Neurophysiol. 2009, 102:979-991.
50. Sakata J.T., Brainard M.S. Real-time contributions of auditory feedback to avian vocal motor control. J. Neurosci. 2006, 26:9619-9628.
51. Sakata J.T., Brainard M.S. Online contributions of auditory feedback to neural activity in avian song control circuitry. J. Neurosci. 2008, 28:11378-11390.
52. Sanes D.H., Bao S. Tuning up the developing auditory CNS. Curr. Opin. Neurobiol. 2009, 19:188-199.
53. 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. 1991, 11:2896-2913.
54. Seki S., Eggermont J.J. Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss. Hear. Res. 2003, 180:28-38.
55. Shibata D.K. Differences in brain structure in deaf persons on MR imaging studied with voxel-based morphometry. AJNR Am. J. Neuroradiol. 2007, 28:243-249.
56. Smith K.M., Mecoli M.D., Altaye M., Komlos M., Maitra R., Eaton K.P., Egelhoff J.C., Holland S.K. Morphometric differences in the Heschl's gyrus of hearing impaired and normal hearing infants. Cereb. Cortex 2011, 21:991-998.
57. Tchernichovski O., Nottebohm F., Ho C.E., Pesaran B., Mitra P.P. A procedure for an automated measurement of song similarity. Anim. Behav. 2000, 59:1167-1176.
58. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002, 420:788-794.
59. Turrigiano G.G., Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 2004, 5:97-107.
60. Vates G.E., Broome B.M., Mello C.V., Nottebohm F. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches. J. Comp. Neurol. 1996, 366:613-642.
61. Waldstein R.S. Effects of postlingual deafness on speech production: implications for the role of auditory feedback. J. Acoust. Soc. Am. 1990, 88:2099-2114.
62. Walmsley B., Berntson A., Leao R.N., Fyffe R.E. Activity-dependent regulation of synaptic strength and neuronal excitability in central auditory pathways. J. Physiol. 2006, 572:313-321.
63. Williams H., McKibben J.R. Changes in stereotyped central motor patterns controlling vocalization are induced by peripheral nerve injury. Behav. Neural Biol. 1992, 57:67-78.
64. Williams H., Mehta N. Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production. J. Neurobiol. 1999, 39:14-28.
65. Woolley S.M., Rubel E.W. Bengalese finches Lonchura Striata domestica depend upon auditory feedback for the maintenance of adult song. J. Neurosci. 1997, 17:6380-6390.
66. Zhou Q., Homma K.J., Poo M.M. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 2004, 44:749-757.
67. Zuo Y., Yang G., Kwon E., Gan W.B. Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 2005, 436:261-265.