Enriched expression and developmental regulation of the middle-weight neurofilament (NF-M) gene in song control nuclei of the zebra finch

Journal of Comparative Neurology

Volumn 500, Issue 3, 2007, Pages 477-497

  Velho, Tarciso A F ^a   Lovell, Peter ^a   Mello, Claudio V ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Neurofilament; Song development; Songbird; Vocal learning

Indexed keywords

CELL MARKER; NEUROFILAMENT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZENK; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; EARLY GROWTH RESPONSE FACTOR 1; EGR1 PROTEIN, MOUSE; NEUROFILAMENT PROTEIN M;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; BRAIN NUCLEUS; CONTROLLED STUDY; CYTOARCHITECTURE; CYTOSKELETON; DEVELOPMENTAL GENETICS; FEMALE; FINCH; GENE EXPRESSION REGULATION; MALE; MEDULLA OBLONGATA; MESENCEPHALON; NEUROFILAMENT; NF M GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PONS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY MECHANISM; SINGING; SONGBIRD; STRUCTURAL GENE; THALAMUS; TRANSCRIPTION REGULATION; ANIMAL; AUDITORY NERVOUS SYSTEM; BRAIN; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LEARNING; METABOLISM; NERVE CELL; PHYSIOLOGY; SEXUAL BEHAVIOR; ULTRASTRUCTURE; VOCALIZATION;

ANIMALS; AUDITORY PATHWAYS; BIOLOGICAL MARKERS; BRAIN; CELL DIFFERENTIATION; CYTOSKELETON; EARLY GROWTH RESPONSE PROTEIN 1; FEMALE; FINCHES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LEARNING; MALE; NEUROFILAMENT PROTEINS; NEURONS; SEXUAL BEHAVIOR, ANIMAL; VOCALIZATION, ANIMAL;

EID: 33846979773     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21180     Document Type: Article

References (113)

1. Akutagawa E, Konishi M. 1998. Transient expression and transport of brain-derived neurotrophic factor in the male zebra finch's song system during vocal development. Proc Natl Acad Sci U S A 95:11429-11434.
2. Akutagawa E, Konishi M. 2001. A monoclonal antibody specific to a song system nuclear antigen in estrildine finches. Neuron 31:545-556.
3. Alvarez-Buylla A, Kirn JR. 1997. Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J Neurobiol 33:585-601.
4. Alvarez-Buylla A, Theelen M, Nottebohm F. 1988. Mapping of radial glia and of a new cell type in adult canary brain. J Neurosci 8:2707-2712.
5. Bailey DJ, Wade J. 2003. Differential expression of the immediate early genes FOS and ZENK following auditory stimulation in the juvenile male and female zebra finch. Brain Res Mol Brain Res 116:147-154.
6. Ball GF. 1994. Neurochemical specializations associated with vocal learning and production in songbirds and budgerigars. Brain Behav Evol 44:234-246.
7. Balthazart J, Foidart A, Wilson EM, Ball GF. 1992. Immunocytochemical localization of androgen receptors in the male songbird and quail brain. J Comp Neurol 317:407-420.
8. Bohner J. 1990. Early acquisition of song in the zebra finch, Taeniopygia guttata. Anim Behav 39:369-374.
9. Boire D, Desgent S, Matteau I, Ptito M. 2005. Regional analysis of neurofilament protein immunoreactivity in the hamster's cortex. J Chem Neuroanat 29:193-208.
10. Bolhuis JJ, Zijlstra GG, den Boer-Visser AM, Van Der Zee EA. 2000. Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc Natl Acad Sci U S A 97:2282-2285.
11. Bottjer SW. 2004. Developmental regulation of basal ganglia circuitry during the sensitive period for vocal learning in songbirds. Ann N Y Acad Sci 1016:395-415.
12. Bottjer SW, Alexander G. 1995. Localization of met-enkephalin and vasoactive intestinal polypeptide in the brains of male zebra finches. Brain Behav Evol 45:153-177.
13. Bottjer SW, Johnson F. 1997. Circuits, hormones, and learning: vocal behavior in songbirds. J Neurobiol 33:602-618.
14. Bottjer SW, Miesner EA, Arnold AP. 1984. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224:901-903.
15. Bottjer SW, Glaessner SL, Arnold AP. 1985. Ontogeny of brain nuclei controlling song learning and behavior in zebra finches. J Neurosci 5:1556-1562.
16. Bottjer SW, Miesner EA, Arnold AP. 1986. Changes in neuronal number, density and size account for increases in volume of song-control nuclei during song development in zebra finches. Neurosci Lett 67:263-268.
17. Bottjer SW, Halsema KA, Brown SA, Miesner EA. 1989. Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J Comp Neurol 279:312-326.
18. Bottjer SW, Brady JD, Cribbs B. 2000. Connections of a motor cortical region in zebra finches: relation to pathways for vocal learning. J Comp Neurol 420:244-260.
19. Brenowitz EA, Margoliash D, Nordeen KW. 1997a. An introduction to birdsong and the avian song system. J Neurobiol 33:495-500.
20. Brenowitz EA, Margoliash D, Nordeen KW. 1997b. The neurobiology of birdsong. J Neurobiol 33:495-710.
21. Canady RA, Burd GD, DeVoogd TJ, Nottebohm F. 1988. Effect of testosterone on input received by an identified neuron type of the canary song system: a Golgi/electron microscopy/degeneration study. J Neurosci 8:3770-3784.
22. Chaudhuri A, Zangenehpour S, Matsubara JA, Cynader MS. 1996. Differential expression of neurofilament protein in the visual system of the vervet monkey. Brain Res 709:17-26.
23. Christy B, Nathans D. 1989. DNA binding site of the growth factor-inducible protein Zif268. Proc Natl Acad Sci U S A 86:8737-8741.
24. Clayton DF. 1997. Role of gene regulation in song circuit development and song learning. J Neurobiol 33:549-571.
25. Denisenko-Nehrbass NI, Jarvis E, Scharff C, Nottebohm F, Mello CV. 2000. Site-specific retinoic acid production in the brain of adult song-birds. Neuron 27:359-370.
26. Durand SE, Heaton JT, Amateau SK, Brauth SE. 1997. Vocal control pathways through the anterior forebrain of a parrot (Melopsittacus undulatuss). J Comp Neurol 377:179-206.
27. Dutar P, Vu HM, Perkel DJ. 1998. Multiple cell types distinguished by physiological, pharmacological, and anatomic properties in nucleus HVc of the adult zebra finch. J Neurophysiol 80:1828-1838.
28. Eales LA. 1985. Song learning in zebra finches: some effects of song model availability on what is learnt and when. Anim Behav 33:1293-1300.
29. Eales LA. 1987. Song learning in female-raised zebra finchs: another look at the sensitive phase. Anim Behav 35:1356-1365.
30. Elder GA, Friedrich VL Jr, Margita A, Lazzarini RA. 1999a. Age-related atrophy of motor axons in mice deficient in the mid-sized neurofilament subunit. J Cell Biol 146:181-192.
31. Elder GA, Friedrich VL Jr, Pereira D, Tu PH, Zhang B, Lee VM, Lazzarini RA. 1999b. Mice with disrupted midsized and heavy neurofilament genes lack axonal neurofilaments but have unaltered numbers of axonal microtubules. J Neurosci Res 57:23-32.
32. Foster EF, Bottjer SW. 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.
33. Gahr M. 2000. Neural song control system of hummingbirds: comparison to swifts, vocal learning (songbirds) and nonlearning (suboscines) passerines, and vocal learning (budgerigars) and nonlearning (dove, owl, gull, quail, chicken) nonpasserines. J Comp Neurol 426:182-196.
34. Gahr M, Metzdorf R. 1999. The sexually dimorphic expression of androgen receptors in the song nucleus hyperstriatalis ventrale pars caudale of the zebra finch develops independently of gonadal steroids. J Neurosci 19:2628-2636.
35. George JM, Clayton DF. 1992. Differential regulation in the avian song control circuit of an mRNA predicting a highly conserved protein related to protein kinase C and the bcr oncogene. Brain Res Mol Brain Res 12:323-329.
36. George JM, Jin H, Woods WS, Clayton DF. 1995. Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron 15:361-372.
37. Gervasi C, Szaro BG. 1997. Sequence and expression patterns of two forms of the middle molecular weight neurofilament protein (NF-M) of Xenopus laevis. Brain Res Mol Brain Res 48:229-242.
38. Glasgow E, Hall CM, Schechter N. 1994. Organization, sequence, and expression of a gene encoding goldfish neurofilament medium protein. J Neurochem 63:52-61.
39. Gurney ME. 1981. Hormonal control of cell form and number in the zebra finch song system. J Neurosci 1:658-673.
40. Haesler S, Wada K, Nshdejan A, Morrisey EE, Lints T, Jarvis ED, Scharff C. 2004. FoxP2 expression in avian vocal learners and nonlearners. J Neurosci 24:3164-3175.
41. Hof PR, Sherwood CC. 2005. Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec A Discov Mol Cell Evol Biol 287:1153-1163.
42. Hof PR, Glezer, II, Archin N, Janssen WG, Morgane PJ, Morrison JH. 1992. The primary auditory cortex in cetacean and human brain: a comparative analysis of neurofilament protein-containing pyramidal neurons. Neurosci Lett 146:91-95.
43. Hof PR, Nimchinsky EA, Morrison JH. 1995. Neurochemical phenotype of corticocortical connections in the macaque monkey: quantitative analysis of a subset of neurofilament protein-immunoreactive projection neurons in frontal, parietal, temporal, and cingulate cortices. J Comp Neurol 362:109-133.
44. Holzenberger M, Jarvis ED, Chong C, Grossman M, Nottebohm F, Scharff C. 1997. Selective expression of insulin-like growth factor II in the songbird brain. J Neurosci 17:6974-6987.
45. Hornung JP, Riederer BM. 1999. Medium-sized neurofilament protein related to maturation of a subset of cortical neurons. J Comp Neurol 414:348-360.
46. Immelmann K. 1969. Song development in the zebra finch and other estrilid finches. In: Hinde RA, editor. Bird vocalizations. Cambridge: Cambridge University Press. p 61-74.
47. Iyengar S, Viswanathan SS, Bottjer SW. 1999. Development of topography within song control circuitry of zebra finches during the sensitive period for song learning. J Neurosci 19:6037-6057.
48. Jarvis ED, Mello CV. 2000. Molecular mapping of brain areas involved in parrot vocal communication. J Comp Neurol 419:1-31.
49. Jarvis ED, Nottebohm F. 1997. Motor-driven gene expression. Proc Natl Acad Sci U S A 94:4097-4102.
50. Jarvis ED, Ribeiro S, da Silva ML, Ventura D, Vielliard J, Mello CV. 2000. Behaviourally driven gene expression reveals song nuclei in hummingbird brain. Nature 406:628-632.
51. Jarvis ED, Gunturkun O, Bruce L, Csillag A, Karten H, Kuenzel W, Medina L, Paxinos G, Perkel DJ, Shimizu T, Striedter G, Wild JM, Ball GF, Dugas-Ford J, Durand SE, Hough GE, Husband S, Kubikova L, Lee DW, Mello CV, Powers A, Siang C, Smulders TV, Wada K, White SA, Yamamoto K, Yu J, Reiner A, Butler AB. 2005. Avian brains and a new understanding of vertebrate brain evolution. Nat Rev Neurosci 6:151-159.
52. Johnson F, Sablan MM, Bottjer SW. 1995. Topographic organization of a forebrain pathway involved with vocal learning in zebra finches. J Comp Neurol 358:260-278.
53. Kaas JH, Collins CE. 2001. The organization of sensory cortex. Curr Opin Neurobiol 11:498-504.
54. Karten HJ. 1968. The ascending auditory pathway in the pigeon (Columba livia). II. Telencephalic projections of the nucleus ovoidalis thalami. Brain Res 11:134-153.
55. Karten HJ. 1997. Evolutionary developmental biology meets the brain: the origins of mammalian cortex. Proc Natl Acad Sci USA 94:2800-2804.
56. Karten HJ, Hodos W. 1967. A stereotaxic atlas of the brain of the pigeon (Columba livia). Baltimore, MD: Johns Hopkins Press.
57. Karten HJ, Shimizu T. 1989. The origins of neocortex: connections and lamination as distinct events in evolution. J Cogn Neurosci 1:291-301.
58. Kelley DB, Nottebohm F. 1979. Projections of a telencephalic auditory nucleus - field L - in the canary. J Comp Neurol 183:455-469.
59. Kimpo RR, Doupe AJ. 1997. FOS is induced by singing in distinct neuronal populations in a motor network. Neuron 18:315-325.
60. Knapska E, Kaczmarek L. 2004. A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/Krox-24/TIS8/ZENK? Prog Neurobiol 74:183-211.
61. Konishi M, Akutagawa E. 1985. Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature 315:145-147.
62. Konishi M, Akutagawa E. 1990. Growth and atrophy of neurons labeled at their birth in a song nucleus of the zebra finch. Proc Natl Acad Sci U S A 87:3538-3541.
63. Korsia S, Bottjer SW. 1989. Developmental changes in the cellular composition of a brain nucleus involved with song learning in zebra finches. Neuron 3:451-460.
64. Kroodsma DE, Konishi M. 1991. A suboscine bird (eastern phoebe, Sayornis phoebe) develops normal song without auditory feedback. Anim Behav 42:477-487.
65. Kuenzel WJ, Masson M. 1988. A stereotaxic atlas of the brain of the chick (Gallus domesticus). Baltimore, MD: Johns Hopkins University Press.
66. Kure R, Brown IR. 1995. Expression of low-molecular-weight neurofilament (NF-L) mRNA during postnatal development of the mouse brain. Neurochem Res 20:833-846.
67. Lee MK, Cleveland DW. 1996. Neuronal intermediate filaments. Annu Rev Neurosci 19:187-217.
68. Luo M, Perkel DJ. 1999. Long-range GABAergic projection in a circuit essential for vocal learning. J Comp Neurol 403:68-84.
69. Luo M, Ding L, Perkel DJ. 2001. An avian basal ganglia pathway essential for vocal learning forms a closed topographic loop. J Neurosci 21:6836-6845.
70. Medina L, Reiner A. 2000. Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:1-12.
71. Mello CV, Clayton DF. 1994. Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J Neurosci 14:6652-6666.
72. Mello CV, Clayton DF. 1995. Differential induction of the ZENK gene in the avian forebrain and song control circuit after metrazole-induced depolarization. J Neurobiol 26:145-161.
73. Mello CV, Ribeiro S. 1998. ZENK protein regulation by song in the brain of songbirds. J Comp Neurol 393:426-438.
74. Mello CV, Vicario DS, Clayton DF. 1992. Song presentation induces gene expression in the songbird forebrain. Proc Natl Acad Sci U S A 89:6818-6822.
75. Mello CV, Jarvis ED, Denisenko N, Rivas M. 1997. Isolation of song-regulated genes in the brain of songbirds. Methods Mol Biol 85:205-217.
76. Metzdorf R, Gahr M, Fusani L. 1999. Distribution of aromatase, estrogen receptor, and androgen receptor mRNA in the forebrain of songbirds and nonsongbirds. J Comp Neurol 407:115-129.
77. Nastiuk KL, Clayton DF. 1995. The canary androgen receptor mRNA is localized in the song control nuclei of the brain and is rapidly regulated by testosterone. J Neurobiol 26:213-224.
78. Nastiuk KL, Mello CV, George JM, Clayton DF. 1994. Immediate-early gene responses in the avian song control system: cloning and expression analysis of the canary c-jun cDNA. Brain Res Mol Brain Res 27:299-309.
79. Nottebohm F. 1972. The origins of vocal learning. Am Naturalist 106:116-140.
80. Nottebohm F, Arnold AP. 1976. Sexual dimorphism in vocal control areas of the songbird brain. Science 194:211-213.
81. Nottebohm F, Stokes TM, Leonard CM. 1976. Central control of song in the canary, Serinus canarius. J Comp Neurol 165:457-486.
82. Nottebohm F, Kelley DB, Paton JA. 1982. Connections of vocal control nuclei in the canary telencephalon. J Comp Neurol 207:344-357.
83. Ohara O, Gahara Y, Miyake T, Teraoka H, Kitamura T. 1993. Neurofilament deficiency in quail caused by nonsense mutation in neurofilament-L gene. J Cell Biol 121:387-395.
84. Price P. 1979. Developmenteal determinants of structure in zebra finch song. J Comp Physiol Psychol 93:260-277.
85. 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. 2004. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414.
86. Riters LV, Ball GF. 2002. Sex differences in the densities of alpha 2-adrenergic receptors in the song control system, but not the medial preoptic nucleus in zebra finches. J Chem Neuroanat 23:269-277.
87. Sakaguchi H, Saito N. 1989. The acetylcholine and catecholamine contents in song control nuclei of zebra finch during song ontogeny. Brain Res Dev Brain Res 47:313-317.
88. Sakaguchi H, Saito N. 1991. Developmental change of cholinergic activity in the forebrain of the zebra finch during song learning. Brain Res Dev Brain Res 62:223-228.
89. Sakaguchi T, Okada M, Kitamura T, Kawasaki K. 1993. Reduced diameter and conduction velocity of myelinated fibers in the sciatic nerve of a neurofilament-deficient mutant quail. Neurosci Lett 153:65-68.
90. Scharff C, Nottebohm F. 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.
91. Schlinger BA, Arnold AP. 1991. Androgen effects on the development of the zebra finch song system. Brain Res 561:99-105.
92. Simpson HB, Vicario DS. 1991. Early estrogen treatment of female zebra finches masculinizes the brain pathway for learned vocalizations. J Neurobiol 22:777-793.
93. Sockman KW, Gentner TQ, Ball GF. 2004. Complementary neural systems for the experience-dependent integration of mate-choice cues in European starlings. J Neurobiol 62:72-81.
94. Soderstrom K, Tian Q, Valenti M, Di Marzo V. 2004. Endocannabinoids link feeding state and auditory perception-related gene expression. J Neurosci 24:10013-10021.
95. Sohrabji F, Nordeen EJ, Nordeen KW. 1990. Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behav Neural Biol 53:51-63.
96. Spiro JE, Dalva MB, Mooney R. 1999. Long-range inhibition within the zebra finch song nucleus RA can coordinate the firing of multiple projection neurons. J Neurophysiol 81:3007-3020.
97. Teramitsu I, Kudo LC, London SE, Geschwind DH, White SA. 2004. Parallel FoxP1 and FoxP2 expression in songbird and human brain predicts functional interaction. J Neurosci 24:3152-3163.
98. Trojanowski JQ, Walkenstein N, Lee VM. 1986. Expression of neurofilament subunits in neurons of the central and peripheral nervous system: an immunohistochemical study with monoclonal antibodies. J Neurosci 6:650-660.
99. van der Gucht E, Vandesande F, Arckens L. 2001. Neurofilament protein: a selective marker for the architectonic parcellation of the visual cortex in adult cat brain. J Comp Neurol 441:345-368.
100. Vates GE, Broome BM, Mello CV, Nottebohm F. 1996. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches. J Comp Neurol 366:613-642.
101. Vates GE, Vicario DS, Nottebohm F. 1997. Reafferent thalamo- "cortical" loops in the song system of oscine songbirds. J Comp Neurol 380:275-290.
102. Velho TA, Pinaud R, Rodrigues PV, Mello CV. 2005. Co-induction of activity-dependent genes in songbirds. Eur J Neurosci 22:1667-1678.
103. Verge VM, Tetzlaff W, Bisby MA, Richardson PM. 1990. Influence of nerve growth factor on neurofilament gene expression in mature primary sensory neurons. J Neurosci 10:2018-2025.
104. Wada K, Sakaguchi H, Jarvis ED, Hagiwara M. 2004. Differential expression of glutamate receptors in avian neural pathways for learned vocalization. J Comp Neurol 476:44-64.
105. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. 2004. Epigenetic programming by maternal behavior. Nat Neurosci 7:847-854.
106. White SA. 2001. Learning to communicate. Curr Opin Neurobiol 11:510-520.
107. Wild JM. 1997. Neural pathways for the control of birdsong production. J Neurobiol 33:653-670.
108. Wild JM, Karten HJ, Frost BJ. 1993. Connections of the auditory forebrain in the pigeon (Columba livia). J Comp Neurol 337:32-62.
109. Yamasaki H, Bennett GS, Itakura C, Mizutani M. 1992. Defective expression of neurofilament protein subunits in hereditary hypotrophic axonopathy of quail. Lab Invest 66:734-743.
110. Zeigler HP, Marler P. 2004. Behavioral neurology of birdsong. New York: New York Academy of Sciences. 788 p.
111. Zhao Y, Szaro BG. 1997. Xefiltin, a new low molecular weight neuronal intermediate filament protein of Xenopus laevis, shares sequence features with goldfish gefiltin and mammalian alpha-internexin and differs in expression from XNIF and NF-L. J Comp Neurol 377:351-364.
112. Zopf D, Hermans-Borgmeyer I, Gundelfinger ED, Betz H. 1987. Identification of gene products expressed in the developing chick visual system: characterization of a middle-molecular-weight neurofilament cDNA. Genes Dev 1:699-708.
113. Zopf D, Dineva B, Betz H, Gundelfinger ED. 1990. Isolation of the chicken middle-molecular weight neurofilament (NF-M) gene and characterization of its promoter. Nucleic Acids Res 18:521-529.