Exploring the zebra finch Taeniopygia guttata as a novel animal model for the speech-language deficit of fragile X syndrome

Results and Problems in Cell Differentiation

Volumn 54, Issue , 2012, Pages 181-197

  Winograd, Claudia ^a   Ceman, Stephanie ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN;

ANIMAL; ARTICLE; DISEASE MODEL; FINCH; FRAGILE X SYNDROME; GENE SILENCING; GENETICS; HISTOLOGY; HUMAN; LANGUAGE DISABILITY; LEARNING; METABOLISM; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; SPEECH DISORDER; VOCALIZATION;

ANIMALS; DISEASE MODELS, ANIMAL; FINCHES; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GENE KNOCKDOWN TECHNIQUES; HUMANS; LANGUAGE DISORDERS; LEARNING; PHENOTYPE; SPEECH DISORDERS; VOCALIZATION, ANIMAL;

EID: 80455125804     PISSN: 00801844     EISSN: 18610412     Source Type: Book Series    
DOI: 10.1007/978-3-642-21649-7_10     Document Type: Article

References (110)

1. Abbeduto L, Murphy MM, Kover ST, Giles ND, Karadottir S, Amman A, Bruno L, Kim JS, Schroeder S, Anderson JA, Nollin KA (2008) Signaling noncomprehension of language: a comparison of fragile X syndrome and Down syndrome. Am J Ment Retard 113:214-230
2. Antar LN, Afroz R, Dictenberg JB, Carroll RC, Bassell GJ (2004) Metabotropic glutamatereceptor activation regulates fragile X mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J Neurosci 24:2648-2655
3. Antar LN, Dictenberg JB, Plociniak M, Afroz R, Bassell GJ (2005) Localization of FMRPassociated mRNA granules and requirement of microtubules for activity-dependent trafficking in hippocampal neurons. Genes Brain Behav 4:350-359
4. Antar LN, Li C, Zhang H, Carroll RC, Bassell GJ (2006) Local functions for FMRP in axon growth cone motility and activity-dependent regulation of filopodia and spine synapses. Mol Cell Neurosci 32:37-48
5. Ashmore RC, Wild JM, Schmidt MF (2005) Brainstem and forebrain contributions to the generation of learned motor behaviors for song. J Neurosci 25:8543-8554
6. Bachner D, Steinbach P, Worhle D, Just W, Vogel M, Hameister H (1993) Enhanced FMR1 expression in testes. Nat Genet 4:155-161
7. Bailey DBJ, Skinner D, Sparkman KL (2003) Discovering fragile X syndrome: family experiences and perceptions. Pediatrics 111:407-416
8. Barnes EF, Roberts J, Mirrett P, Sideris J, Misenheimer J (2006) A comparison of oral structure and oral-motor function in young males with fragile X syndrome and Down syndrome. J Speech Lang Hear Res 49:903-917
9. Barnes E, Roberts J, Long SH, Martin GE, Berni MC, Mandulak KC, Sideris J (2009) Phonological accuracy and intelligibility in connected speech of boys with fragile X syndrome or Down syndrome. J Speech Lang Hear Res 52:1048-1061
10. Bear MF, Huber KM, Warren ST (2004) The mGluR theory of fragile X mental retardation. Trends Neurosci 27:370-377
11. Belser RC, Sudhalter V (2001) Conversational characteristics of children with fragile X syndrome: repetitive speech. Am J Ment Retard 106:28-38
12. Bohn MC (2005) Overview of gene therapy and viral vectors for CNS applications. Society for Neuroscience (Short Course), Washington, DC
13. Bottjer SW (2005) Silent synapses in a thalamo-cortical circuit necessary for song learning in zebra finches. J Neurophysiol 94:3698-3707
14. Brady N, Skinner D, Roberts J, Hennon E (2006) Communication in young children with fragile X syndrome: a qualitative study of mothers' perspectives. Am J Speech Lang Pathol 15:353-364
15. Brainard MS, Doupe AJ (2001) Postlearning consolidation of birdson: stabilizing effects of age and anterior forebrain lesions. J Neurosci 21:2501-2517
16. Brainard MS, Doupe AJ (2002) What songbirds teach us about learning. Nature 417:351-358
17. Branchi I, Santucci D, Alleva E (2001) Ultrasonic vocalisation emitted by infant rodents: a tool for assessment of neurobehavioural development. Behav Brain Res 125:49-56
18. Ching TY, Crowe K, Martin V, Day J, Mahler N, Youn S, Street L, Cook C, Orsini J (2010) Language development and everyday functioning of children with hearing loss assessed at 3 years of age. Int J Speech Lang Pathol 12:124-131
19. Consortium D-BFX (1994) FMR1 knockout mice: a model to study fragile X mental retardation. Cell 78:23-33
20. Dalton KM, Holsen L, Abbeduto L, Davidson RJ (2008) Brain function and gaze fixation during facial-emotion processing in fragile X and autism. Autism Res 1:231-239
21. De Boulle K, Verkerk AJMH, Reyniers E, Vits L, Hendrickx J, Van Roy B, Van den Bos F, de Graaff E, Oostra BA, Willems PJ (1993) A point mutation in the FMR-1 gene associated with fragile X mental retardation. Nat Genet 3:31-35
22. Devys D, Lutz Y, Rouyer N, Bellocq J-P, Mandel J-L (1993) The FMR-1 protein is cytoplasmic, most abundant in neurons, and appears normal in carriers of the fragile X premutation. Nat Genet 4:335-340
23. Ding L, Perkel DJ, Farries MA (2003) Presynaptic depression of glutamatergic synaptic transmission by D1-like dopamine receptor activation in the avian basal ganglia. J Neurosci 23:6086-6095
24. Doupe AJ, Kuhl PK (1999) Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 22:567-631
25. Eadie BD, Cushman J, Kannangara TS, Fanselow MS, Christie BR (2010) NMDA receptor hypofunction in the dentate gyrus and impaired context discrimination in adult Fmr1 knockout mice. Hippocampus. Ahead of print
26. Edbauer D, Neilson JR, Foster KA, Wang CF, Seeburg DP, Batterton MN, Tada T, Dolan BM, Sharp PA, Sheng M (2010) Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65:373-384
27. Farries MA, Perkel DJ (2002) A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus. J Neurosci 22:3776-3787
28. Fee MS, Kozhevnikov A, Hahnloser R (2004) Neural mechanisms of vocal sequence generation in the songbird. Ann N Y Acad Sci 1016:153-170
29. Feng Y, Gutekunst CA, Eberhart DE, Yi H, Warren ST, Hersch SM (1997) Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J Neurosci 17:1539-1547
30. Ferrando-Lucas MT, Banús-Gómez P, López-Pérez G (2003) Aspects of cognition and language in children with fragile X syndrome. Rev Neurol 36(Suppl 1):S137-S142
31. Ferrier LJ, Bashir AS, Meryash DL, Johnston J, Wolff P (1991) Conversational skills of individuals with fragile-X syndrome: a comparison with autism and Down syndrome. Dev Med Child Neurol 33:776-788
32. Fiete IR, Fee MS, Seung HS (2007) Model of birdsong learning based on gradient estimation by dynamic perturbation of neural conductances. J Neurophysiol 98:2038-2057
33. Finestack LH, Richmond EK, Abbeduto L (2009) Language development in individuals with fragile X syndrome. Top Lang Disord 29:133-148
34. Grace TB, Cassandra DD, Martie LS, Donald B Jr, Hatton DD, Jane ER, Penny LM (2005) Video analysis of sensory-motor features in infants with fragile X syndrome at 9-12 months of age. J Autism Dev Disord 35:645
35. GreenoughWT, Klintsova AY, Irwin SA, Galvez R, Bates KE, Weiler IJ (2001) Synaptic regulation of protein synthesis and the fragile X protein. Proc Natl Acad Sci USA 98:7101-7106
36. Haesler S, Wada K, Nshdejan A, Morrisey EE, Lints T, Jarvis ED, Scharff C (2004) FoxP2 expression in avian vocal learners and non-learners. J Neurosci 24:3164-3175
37. Haesler S, Rochefort C, Georgi B, Licznerski P, Osten P, Scharff C (2007) Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X. PLoS Biol 5:2885-2897
38. Hagerman RJ, Lampe ME (1999) Handbook of neurodevelopmental and genetic disorders in children. Guilford Press, New York
39. Hagerman RJ, Staley LW, O'Conner R, Lugenbeel K, Nelson D, McLean SD, Taylor A (1996) Learning-disabled males with a fragile X CGG expansion in the upper premutation size range. Pediatrics 97:122-126
40. Hagerman RJ, Berry-Kravis E, Kaufmann WE, Ono MY, Tartaglia N, Lachiewicz A, Kronk R, Delahunty C, Hessl D, Visootsak J, Picker J, Gane L, Tranfaglia M (2009) Advances in the treatment of fragile X syndrome. Pediatrics 123:378-390
41. Hamada A, Miyawaki K, Honda-sumi E, Tomioka K, Mito T, Ohuchi H, Noji S (2009) Loss-of-function analyses of the fragile X-related and dopamine receptor genes by RNA interference in the cricket Gryllus bimaculatus. Dev Dyn 238:2025-2033
42. Harper SQ, Staber PD, He X, Eliason SL, Martins IH, Mao Q, Yang L, Kotin RM, Paulson HL, Davidson BL (2005) RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc Natl Acad Sci USA 102:5820-5825
43. Hergersberg M, Matsuo K, Gassman M, Schaffner W, Lüscher B, Rülicke T, Aguzzi A (1995) Tissue-specific expression of a FMR1/beta-galactosidase fusion gene in transgenic mice. Hum Mol Genet 4:359-366
44. Hodge MM (1991) Assessing early speech motor function. Clin Commun Disord 1:69-85
45. Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3:e386
46. Kao MH, Doupe AJ, Brainard MS (2005) Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433:638-643
47. Kau AS, Meyer WA, Kaufmann WE (2002) Early development in males with fragile X syndrome: a review of the literature. Microsc Res Tech 57:174-178
48. Ke J-Y, Chen C-L, Chen Y-J, Chen C-H, Lee L-F, Chiang T-M (2005) Features of developmental functions and autistic profiles in children with fragile X syndrome. Chang Gung Med J 28:551-558
49. Konishi M, Akutagawa E (1985) Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch. Nature 315:145-147
50. Kover ST, Abbeduto L (2010) Expressive language in male adolescents with fragile X syndrome with and without comorbid autism. J Intellect Disabil Res 54:246-265
51. Lai CS, Fisher SE, Hurst JA, Vargha-Khadem F, Monaco AP (2001) A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413:519-523
52. Lewis P, Abbeduto L, Murphy M, Richmond E, Giles N, Bruno L, Schroeder S (2006) Cognitive, language and social-cognitive skills of individuals with fragile X syndrome with and without autism. J Intellect Disabil Res 50:532-545
53. Lin SL, Chang SJ, Ying SY (2006) First in vivo evidence of microRNA-induced fragile X mental retardation syndrome. Mol Psychiatry 11:616-617
54. Ling SC, Fahrner PS, Greenough WT, Gelfand VI (2004) Transport of Drosophila fragile X mental retardation protein-containing ribonucleoprotein granules by kinesin-1 and cytoplasmic dynein. Proc Natl Acad Sci USA 101:17428-17433
55. Livingston FS, Mooney R (1997) Development of intrinsic and synaptic properties in a forebrain nucleus essential to avian song learning. J Neurosci 17:8997-9009
56. Luo M, Perkel DJ (1999) A GABAergic, strongly inhibitory projection to a thalamic nucleus in the zebra finch song system. J Neurosci 19:6700-6711
57. Luo M, Perkel DJ (2002) Intrinsic and synaptic properties of neurons in an avian thalamic nucleus during song learning. J Neurophysiol 88:1903-1914
58. Margoliash D (1997) Functional organization of forebrain pathways for song production and perception. J Neurobiol 33:671-693
59. Marler P, Waser MS (1977) Role of auditory feedback in canary song development. J Comp Physiol Psychol 91:8-16
60. Medina L, Reiner A (1995) Neurotransmitter organization and connectivity of the basal ganglia in vertebrates: implicatios for the evolution of basal ganglia. Brain Behav Evol 46:235-258
61. Mercaldo V, Descalzi G, Zhuo M (2009) Fragile X mental retardation protein in learning-related synaptic plasticity. Mol Cells 28:501-507
62. Michel CI, Kraft R, Restifo LL (2004) Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants. J Neurosci 24:5798-5809
63. Mooney R (1992) Synaptic basis for developmental plasticity in a birdsong nucleus. J Neurosci 12:2464-2477
64. Mooney R, Rao M (1994) Waiting periods versus early innervation: the development of axonal connections in the zebra finch song system. J Neurosci 14:6532-6543
65. Newbury DF, Monaco AP (2010) Genetic advances in the study of speech and language disorders. Neuron 68:309-320
66. Nottebohm F, Stokes TM, Leonard CM (1976) Central control of song in the canary, Serinus canarius. J Comp Neurol 165:457-486
67. Noveck IA, Reboul A (2008) Experimental pragmatics: a Gricean turn in the study of language. Trends Cogn Sci 12:425-431
68. Olveczky BP, Andalman AS, Fee MS (2005) Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol 3:e153
69. Pacey LK, Doering LC (2007) Developmental expression of FMRP in the astrocyte lineage: implications for fragile X syndrome. Glia 55:1601-1609
70. Pieretti M, Zhang F, Fu YH, Warren ST, Oostra BA, Caskey CT, Nelson DL (1991) Absence of expression of the FMR-1 gene in fragile X syndrome. Cell 66:817-822
71. Price TJ, Flores CM, Cervero F, Hargreaves KM (2006) The RNA binding and transport proteins staufen and fragile X mental retardation protein are expressed by rat primary afferent neurons and localize to peripheral and central axons. Neuroscience 141:2107-2116
72. Price J, Roberts J, Vandergrift N, Martin G (2007) Language comprehension in boys with fragile X syndrome and boys with Down syndrome. J Intellect Disabil Res 51:318-326
73. Price JR, Roberts JE, Hennon EA, Berni MC, Anderson KL, Sideris J (2008) Syntactic complexity during conversation of boys with fragile X syndrome and Down syndrome. J Speech Lang Hear Res 51:3-15
74. Ralph GS, Radcliffe PA, Day DM, Carthy JM, Leroux MA, Lee DC, Wong LF, Bilsland LG, Greensmith L, Kingsman SM, Mitrophanous KA, Mazarakis ND, Azzouz M (2005) Silencing mutant SOD1 using RNAi protects against neurodegeneration and extends survival in an ALS model. Nat Med 11:429-433
75. Raoul C, Abbas-Terki T, Bensadoun JC, Guillot S, Haase G, Szulc J, Henderson CE, Aebischer P (2005) Lentiviral-mediated silencing of SOD1 through RNA interference retards disease onset and progression in a mouse model of ALS. Nat Med 11:423-428
76. Reiner A, Perkel DJ, Bruce LL, Butler AB, Csillag A, Kuenzel W, Medina L, Paxinos G, Shimizu T, Striedter G, Wild M, Ball GF, Surand S, Guturkun 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 E (2004a) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J Comp Neurol 473:377-414
77. Reiner A, Perkel DJ, Mello CV, Jarvis ED (2004b) Songbirds and the revised avian brain nomenclature. Ann N Y Acad Sci 1016:77-108
78. Roberts J, Price J, Barnes E, Nelson L, Burchinal M, Hennon EA, Moskowitz L, Edwards A, Malkin C, Anderson K, Misenheimer J, Hooper SR (2007) Receptive vocabulary, expressive vocabulary, and speech production of boys with fragile X syndrome in comparison to boys with down syndrome. Am J Ment Retard 112:177-193
79. Roberts TF, Tschida KA, Klein ME, Mooney R (2010) Rapid spine stabilization and synaptic enhancement at the onset of behavioral learning. Nature 463:948-952
80. Rochefort C, He X, Scotto-Lomassese S, Scharff C (2007) Recruitment of FoxP2-expressing neurons to Area X varies during song development. Dev Neurobiol 67:809-817
81. Rodriguez-Lebron E, Denovan-Wright EM, Nash K, Lewin AS, Mandel RJ (2005) Intrastriatal rAAV-mediated delivery of anti-huntingtin shRNAs induces partial reversal of disease progression in R6/1 Huntington's disease transgenic mice. Mol Ther 12:618
82. Sales G (1972) Ultrasound and mating behavior in rodents with some observations on other behavioural situations. J Zool Lond 168:149-164
83. Sapru MK, Yates JW, Hogan S, Jiang L, Halter J, Bohn MC (2006) Silencing of human [alpha]- synuclein in vitro and in rat brain using lentiviral-mediated RNAi. Exp Neurol 198:382
84. Scharff C, Haesler S (2005) An evolutionary perspective on FoxP2: strictly for the birds? Curr Opin Neurobiol 15:694
85. 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
86. Schulz SB, Haesler S, Scharff C, Rochefort C (2010) Knockdown of FoxP2 alters spine density in Area X of the zebra finch. Genes Brain Behav 9(7):732-740
87. Shu W, Cho JY, Jiang Y, Zhang M, Weisz D, Elder GA, Schmeidler J, De Gasperi R, Sosa MAG, Rabidou D, Santucci AC, Perl D, Morrisey E, Buxbaum JD (2005) Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc Natl Acad Sci USA 102:9643-9648
88. Singer O, Marr RA, Rockenstein E, Crews L, Coufal NG, Gage FH, Verma IM, Masliah E (2005) Targeting BACE1 with siRNAs ameliorates Alzheimer disease neuropathology in a transgenic model. Nat Neurosci 8:1343-1349
89. Siomi MC, Siomi H, Sauer WH, Srinivasan S, Nussbaum RL, Dreyfuss G (1995) FXR1, an autosomal homolog of the fragile X mental retardation protein. EMBO J 14:2401-2408
90. Sossinka R, Bhoner J (1980) Song types in the zebra finch Poephila guttata castanotis. Z Tierpsychol 53:123-132
91. Spencer CM, Serysheva E, Yuva-Paylor LA, Oostra BA, Nelson DL, Paylor R (2006) Exaggerated behavioral phenotypes in Fmr1/Fxr2 double knockout mice reveal a functional genetic interaction between fragile X-related proteins. Hum Mol Genet 15:1984-1994
92. Spiro JE, Dalva MB, Mooney R (1999) Long-rage inhibition within the zebra finch song nucleus RA can coordinate the firing of multiple projection neurons. J Neurophysiol 81:3007-3020
93. Stark LL, Perkel DJ (1999) Two-stage, input-specific synaptic maturation in a nucleus essential for vocal production in the zebra finch. J Neurosci 19:9107-9116
94. Sudhalter V, Cohen IL, Silverman W, Wolf-Schein EG (1990) Conversational analyses of males with fragile X, Down syndrome, and autism: comparison of the emergence of deviant language. Am J Ment Retard 94:431-441
95. Tchernichovski O, Nottebohm F, Ho CE, Pesaran B, Mitra PP (2000) A procedure for an automated measurement of song similarity. Anim Behav 59:1167-1176
96. Tessier CR, Broadie K (2008) Drosophila fragile X mental retardation protein developmentally regulates activity-dependent axon pruning. Development 135:1547-1557
97. Vargha-Khadem F, Watkins K, Alcock K, Fletcher P, Passingham R (1995) Praxic and nonverbal cognitive deficits in a large family with a genetically transmitted speech and language disorder. Proc Natl Acad Sci USA 92:930-933
98. Vilkman E, Niemi J, Ikonen U (1988) Fragile X speech pathology in Finnish. Brain Lang 34:203-221
99. Vu ET, Mazurek ME, Kuo YC (1994) Identification of a forebrain motor programming network for the learned song of zebra finches. J Neurosci 14:6924-6934
100. Wang J, Hessler NA (2006) Coordination of presynaptic and postsynaptic maturation in a zebra finch forebrain motor control nucleus during song learning. Eur J Neurosci 24:2859-2869
101. Wang H, Ku L, Osterhout DJ, Li W, Ahmadian A, Liang Z, Feng Y (2004) Developmentallyprogrammed FMRP expression in oligodendrocytes: a potential role of FMRP in regulating translation in oligodendroglia progenitors. Hum Mol Genet 13:79-89
102. Weiler IJ, Greenough WT (1999) Synaptic synthesis of the fragile X protein: possible involvement in synapse maturation and elimination. Am J Med Genet 83:248-252
103. Weiler IJ, Irwin SA, Klintsova AY, Spencer CM, Brazelton AD, Miyashiro K, Comery TA, Patel B, Eberwine J, Greenough WT (1997) Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc Natl Acad Sci USA 94:5395-5400
104. Wilbrecht L, Nottebohm F (2003) Vocal learning in birds and humans. Ment Retard Dev Disabil Res Rev 9:135-148
105. Winograd C, Clayton D, Ceman S (2008) Expression of fragile X mental retardation protein within the vocal control system of developing and adult male zebra finches. Neuroscience 157:132-142
106. Xia H, Mao Q, Eliason SL, Harper SQ, Martins IH, Orr HT, Paulson HL, Yang L, Kotin RM, Davidson BL (2004) RNAi suppresses polyglutamine-induced neurodegeneration in a model of spinocerebellar ataxia. Nat Med 10:816
107. Zajac DJ, Roberts JE, Hennon EA, Harris AA, Barnes EF, Misenheimer J (2006) Articulation rate and vowel space characteristics of young males with fragile X syndrome: preliminary acoustic findings. J Speech Lang Hear Res 49:1147-1155
108. Zajac DJ, Harris AA, Roberts JE, Martin GE (2009) Direct magnitude estimation of articulation rate in boys with fragile X syndrome. J Speech Lang Hear Res 52:1370-1379
109. Zhang YQ, Bailey AM, Matthies HJ, Renden RB, Smith MA, Speese SD, Rubin GM, Broadie K (2001) Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107:591-603
110. Zingerevich C, Greiss-Hess L, Lemons-Chitwood K, Harris SW, Hessl D, Cook K, Hagerman RJ (2009) Motor abilities of children diagnosed with fragile X syndrome with and without autism. J Intellect Disabil Res 53:11-18