Modeling human neurodevelopmental disorders in the Xenopus tadpole: From mechanisms to therapeutic targets

DMM Disease Models and Mechanisms

Volumn 6, Issue 5, 2013, Pages 1057-1065

  Pratt, Kara G ^a   Khakhalin, Arseny S ^b  

^a UNIVERSITY OF WYOMING   (United States)

^b BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTISM; CELL ACTIVITY; CONNECTOME; ENVIRONMENTAL EXPOSURE; EPILEPSY; HOMEOSTASIS; MOLECULAR MECHANICS; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVOUS SYSTEM FUNCTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEIZURE; TADPOLE; XENOPUS;

ANIMALS; DEVELOPMENTAL DISABILITIES; DISEASE MODELS, ANIMAL; ENVIRONMENTAL POLLUTANTS; HUMANS; LARVA; NERVOUS SYSTEM; XENOPUS;

EID: 84883860621     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.012138     Document Type: Review

References (151)

1. Abrahams, B. S. and Geschwind, D. H. (2008). Advances in autism genetics: on the threshold of a new neurobiology. Nat. Rev. Genet. 9, 341-355.
2. Aizenman, C. D. and Cline, H. T. (2007). Enhanced visual activity in vivo forms nascent synapses in the developing retinotectal projection. J. Neurophysiol. 97, 2949-2957.
3. Aizenman, C. D., Muñoz-Elías, G. and Cline, H. T. (2002). Visually driven modulation of glutamatergic synaptic transmission is mediated by the regulation of intracellular polyamines. Neuron 34, 623-634.
4. Aizenman, C. D., Akerman, C. J., Jensen, K. R. and Cline, H. T. (2003). Visually driven regulation of intrinsic neuronal excitability improves stimulus detection in vivo. Neuron 39, 831-842.
5. Akerman, C. J. and Cline, H. T. (2006). Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. J. Neurosci. 26, 5117-5130.
6. Amaya, E., Offield, M. F. and Grainger, R. M. (1998). Frog genetics: Xenopus tropicalis jumps into the future. Trends Genet. 14, 253-255.
7. Amir, R. E., Van den Veyver, I. B., Wan, M., Tran, C. Q., Francke, U. and Zoghbi, H. Y. (1999). Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23, 185-188.
8. Bell, M. R., Belarde, J. A., Johnson, H. F. and Aizenman, C. D. (2011). A neuroprotective role for polyamines in a Xenopus tadpole model of epilepsy. Nat. Neurosci. 14, 505-512.
9. Berg, C., Gyllenhammar, I. and Kvarnryd, M. (2009). Xenopus tropicalis as a test system for developmental and reproductive toxicity. J. Toxicol. Environ. Health A 72, 219-225.
10. Bestman, J. E. and Cline, H. T. (2008). The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo. Proc. Natl. Acad. Sci. USA 105, 20494-20499.
11. Bestman, J. E., Ewald, R. C., Chiu, S. L. and Cline, H. T. (2006). In vivo single-cell electroporation for transfer of DNA and macromolecules. Nat. Protoc. 1, 1267-1272.
12. Bestman, J. E., Lee-Osbourne, J. and Cline, H. T. (2012). In vivo time-lapse imaging of cell proliferation and differentiation in the optic tectum of Xenopus laevis tadpoles. J. Comp. Neurol. 520, 401-433.
13. Bhakar, A. L., Dölen, G. and Bear, M. F. (2012). The pathophysiology of fragile X (and what it teaches us about synapses). Annu. Rev. Neurosci. 35, 417-443.
14. Blonden, L., van't Padje, S., Severijnen, L. A., Destree, O., Oostra, B. A. and Willemsen, R. (2005). Two members of the Fxr gene family, Fmr1 and Fxr1, are differentially expressed in Xenopus tropicalis. Int. J. Dev. Biol. 49, 437-441.
15. Bollmann, J. H. and Engert, F. (2009). Subcellular topography of visually driven dendritic activity in the vertebrate visual system. Neuron 61, 895-905.
16. Butler, M. G., Dasouki, M. J., Zhou, X. P., Talebizadeh, Z., Brown, M., Takahashi, T. N., Miles, J. H., Wang, C. H., Stratton, R., Pilarski, R. et al. (2005). Subset of individuals with autism spectrum disorders and extreme macrocephaly associated with germline PTEN tumour suppressor gene mutations. J. Med. Genet. 42, 318-321.
17. Castoldi, A. F., Coccini, T., Ceccatelli, S. and Manzo, L. (2001). Neurotoxicity and molecular effects of methylmercury. Brain Res. Bull. 55, 197-203.
18. Chen, S. X. and Haas, K. (2011). Function directs form of neuronal architecture. BioArchitecture 1, 2-4.
19. Chen, S. X., Tari, P. K., She, K. and Haas, K. (2010). Neurexin-neuroligin cell adhesion complexes contribute to synaptotropic dendritogenesis via growth stabilization mechanisms in vivo. Neuron 67, 967-983.
20. Chen, S. X., Cherry, A., Tari, P. K., Podgorski, K., Kwong, Y. K. and Haas, K. (2012). The transcription factor MEF2 directs developmental visually driven functional and structural metaplasticity. Cell 151, 41-55.
21. Cheng, Y., Cui, Y., Chen, H. M. and Xie, W. P. (2011). Thyroid disruption effects of environmental level perfluorooctane sulfonates (PFOS) in Xenopus laevis. Ecotoxicology 20, 2069-2078.
22. Chiu, S. L. and Cline, H. T. (2010). Insulin receptor signaling in the development of neuronal structure and function. Neural Dev. 5, 7.
23. Chiu, S. L., Chen, C. M. and Cline, H. T. (2008). Insulin receptor signaling regulates synapse number, dendritic plasticity, and circuit function in vivo. Neuron 58, 708-719.
24. Cline, H. T. and Kelly, D. (2012). Xenopus as an experimental system for developmental neuroscience: introduction to a special issue. Dev. Neurobiol. 72, 463-464.
25. Cline, H. T., Witte, S. and Jones, K. W. (1996a). Low lead levels stunt neuronal growth in a reversible manner. Proc. Natl. Acad. Sci. USA 93, 9915-9920.
26. Cline, H. T., Wu, G. Y. and Malinow, R. (1996b). In vivo development of neuronal structure and function. Cold Spring Harb. Symp. Quant. Biol. 61, 95-104.
27. Coen, L., Le Blay, K., Rowe, I. and Demeneix, B. A. (2007). Caspase-9 regulates apoptosis/proliferation balance during metamorphic brain remodeling in Xenopus. Proc. Natl. Acad. Sci. USA 104, 8502-8507.
28. Cohen-Cory, S. (2007). Imaging retinotectal synaptic connectivity. CSH Protoc 2007, pdb prot4782
29. Cohly, H. H. and Panja, A. (2005). Immunological findings in autism. Int. Rev. Neurobiol. 71, 317-341.
30. Constantine-Paton, M. and Capranica, R. R. (1976). Axonal guidance of developing optic nerves in the frog. I. Anatomy of the projection from transplanted eye primordia. J. Comp. Neurol. 170, 17-31.
31. Damjanovski, S., Amano, T., Li, Q., Ueda, S., Shi, Y. B. and Ishizuya-Oka, A. (2000). Role of ECM remodeling in thyroid hormone-dependent apoptosis during anuran metamorphosis. Ann. N. Y. Acad. Sci. 926, 180-191.
32. De Robertis, E. M. (2006). Spemann's organizer and self-regulation in amphibian embryos. Nat. Rev. Mol. Cell Biol. 7, 296-302.
33. Deeg, K. E., Sears, I. B. and Aizenman, C. D. (2009). Development of multisensory convergence in the Xenopus optic tectum. J. Neurophysiol. 102, 3392-3404.
34. Degitz, S. J., Durhan, E. J., Tietge, J. E., Kosian, P. A., Holcombe, G. W. and Ankley, G. T. (2003). Developmental toxicity of methoprene and several degradation products in Xenopus laevis. Aquat. Toxicol. 64, 97-105.
35. Demarque, M. and Spitzer, N. C. (2010). Activity-dependent expression of Lmx1b regulates specification of serotonergic neurons modulating swimming behavior. Neuron 67, 321-334.
36. Deverman, B. E. and Patterson, P. H. (2009). Cytokines and CNS development. Neuron 64, 61-78.
37. Dingwell, K. S., Holt, C. E. and Harris, W. A. (2000). The multiple decisions made by growth cones of RGCs as they navigate from the retina to the tectum in Xenopus embryos. J. Neurobiol. 44, 246-259.
38. Dong, W. and Aizenman, C. D. (2012). A competition-based mechanism mediates developmental refinement of tectal neuron receptive fields. J. Neurosci. 32, 16872-16879.
39. Dong, W., Lee, R. H., Xu, H., Yang, S., Pratt, K. G., Cao, V., Song, Y. K., Nurmikko, A. and Aizenman, C. D. (2009). Visual avoidance in Xenopus tadpoles is correlated with the maturation of visual responses in the optic tectum. J. Neurophysiol. 101, 803-815.
40. Dumpert, K. and Zietz, E. (1984). Platanna (Xenopus laevis) as a test organism for determining the embryotoxic effects of environmental chemicals. Ecotoxicol. Environ. Saf. 8, 55-74.
41. Elliott, K. L., Houston, D. W. and Fritzsch, B. (2013). Transplantation of Xenopus laevis tissues to determine the ability of motor neurons to acquire a novel target. PLoS ONE 8, e55541.
42. Engert, F., Tao, H. W., Zhang, L. I. and Poo, M. M. (2002). Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons. Nature 419, 470-475.
43. Feng, J. N., Schroer, R., Yan, J., Song, W. J., Yang, C. M., Bockholt, A., Cook, E. H., Jr, Skinner, C., Schwartz, C. E. and Sommer, S. S. (2006). High frequency of neurexin 1beta signal peptide structural variants in patients with autism. Neurosci. Lett. 409, 10-13.
44. Filoni, S. (2009). Retina and lens regeneration in anuran amphibians. Semin. Cell Dev. Biol. 20, 528-534.
45. Gatto, C. L. and Broadie, K. (2011). Drosophila modeling of heritable neurodevelopmental disorders. Curr. Opin. Neurobiol. 21, 834-841.
46. Gaze, R. M. (1958). The representation of the retina on the optic lobe of the frog. Q. J. Exp. Physiol. Cogn. Med. Sci. 43, 209-214.
47. Geschwind, D. H. (2009). Advances in autism. Annu. Rev. Med. 60, 367-380.
48. Gessert, S., Bugner, V., Tecza, A., Pinker, M. and Kühl, M. (2010). FMR1/FXR1 and the miRNA pathway are required for eye and neural crest development. Dev. Biol. 341, 222-235.
49. Gessert, S., Schmeisser, M. J., Tao, S., Boeckers, T. M. and Kühl, M. (2011). The spatio-temporal expression of ProSAP/shank family members and their interaction partner LAPSER1 during Xenopus laevis development. Dev. Dyn. 240, 1528-1536.
50. Guo, W., Zhang, L., Christopher, D. M., Teng, Z. Q., Fausett, S. R., Liu, C., George, O. L., Klingensmith, J., Jin, P. and Zhao, X. (2011). RNA-binding protein FXR2 regulates adult hippocampal neurogenesis by reducing Noggin expression. Neuron 70, 924-938.
51. Gutleb, A. C., Appelman, J., Bronkhorst, M., van den Berg, J. H. J. and Murk, A. J. (2000). Effects of oral exposure to polychlorinated biphenyls (PCBs) on the development and metamorphosis of two amphibian species (Xenopus laevis and Rana temporaria). Sci. Total Environ. 262, 147-157.
52. Haas, K., Sin, W. C., Javaherian, A., Li, Z. and Cline, H. T. (2001). Single-cell electroporation for gene transfer in vivo. Neuron 29, 583-591.
53. Haas, K., Jensen, K., Sin, W. C., Foa, L. and Cline, H. T. (2002). Targeted electroporation in Xenopus tadpoles in vivo-from single cells to the entire brain. Differentiation 70, 148-154.
54. Harland, R. M. and Grainger, R. M. (2011). Xenopus research: metamorphosed by genetics and genomics. Trends Genet. 27, 507-515.
55. Harris, W. A., Holt, C. E. and Bonhoeffer, F. (1987). Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: a timelapse video study of single fibres in vivo. Development 101, 123-133.
56. Hawley, S. H. B., Wünnenberg-Stapleton, K., Hashimoto, C., Laurent, M. N., Watabe, T., Blumberg, B. W. and Cho, K. W. Y. (1995). Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev. 9, 2923-2935.
57. Hayashi, Y., Hattori, Y., Moriwaki, A., Lu, Y. F. and Hori, Y. (1993). Increases in brain polyamine concentrations in chemical kindling and single convulsion induced by pentylenetetrazol in rats. Neurosci. Lett. 149, 63-66.
58. Helbing, C. C., Bailey, C. M., Ji, L., Gunderson, M. P., Zhang, F., Veldhoen, N., Skirrow, R. C., Mu, R. X., Lesperance, M., Holcombe, G. W. et al. (2007). Identification of gene expression indicators for thyroid axis disruption in a Xenopus laevis metamorphosis screening assay. Part 1. Effects on the brain. Aquat. Toxicol. 82, 227-241.
59. Hellsten, U., Harland, R. M., Gilchrist, M. J., Hendrix, D., Jurka, J., Kapitonov, V., Ovcharenko, I., Putnam, N. H., Shu, S., Taher, L. et al. (2010). The genome of the Western clawed frog Xenopus tropicalis. Science 328, 633-636.
60. Hewapathirane, D. S., Dunfield, D., Yen, W., Chen, S. and Haas, K. (2008). In vivo imaging of seizure activity in a novel developmental seizure model. Exp. Neurol. 211, 480-488.
61. Hiramoto, M. and Cline, H. T. (2009). Convergence of multisensory inputs in Xenopus tadpole tectum. Dev. Neurobiol. 69, 959-971.
62. Holt, C. E. (1989). A single-cell analysis of early retinal ganglion cell differentiation in Xenopus: from soma to axon tip. J. Neurosci. 9, 3123-3145.
63. Holtzman, D. and Hsu, J. S. (1976). Early effects of inorganic lead on immature rat brain mitochondrial respiration. Pediatr. Res. 10, 70-75.
64. Hossain, S., Hewapathirane, D. S. and Haas, K. (2012). Dynamic morphometrics reveals contributions of dendritic growth cones and filopodia to dendritogenesis in the intact and awake embryonic brain. Dev. Neurobiol. 72, 615-627.
65. Huot, M. E., Bisson, N., Davidovic, L., Mazroui, R., Labelle, Y., Moss, T. and Khandjian, E. W. (2005). The RNA-binding protein fragile X-related 1 regulates somite formation in Xenopus laevis. Mol. Biol. Cell 16, 4350-4361.
66. Huot, M. E., Bisson, N., Moss, T. and Khandjian, E. W. (2012). Manipulating the fragile X mental retardation proteins in the frog. Results Probl. Cell Differ. 54, 165-179.
67. Ichtchenko, K., Nguyen, T. and Südhof, T. C. (1996). Structures, alternative splicing, and neurexin binding of multiple neuroligins. J. Biol. Chem. 271, 2676-2682.
68. Imaizumi, K., Shih, J. Y. and Farris, H. E. (2013). Global hyper-synchronous spontaneous activity in the developing optic tectum. Sci Rep 3, 1552.
69. Ishimaru, H., Kamboj, R., Ambrosini, A., Henley, J. M., Soloviev, M. M., Sudan, H., Rossier, J., Abutidze, K., Rampersad, V., Usherwood, P. N. R. et al. (1996). A unitary non-NMDA receptor short subunit from Xenopus: DNA cloning and expression. Receptors Channels 4, 31-49.
70. Jamain, S., Betancur, C., Quach, H., Philippe, A., Fellous, M., Giros, B., Gillberg, C., Leboyer, M., Bourgeron, T.; Paris Autism Research International Sibpair (PARIS) Study (2002). Linkage and association of the glutamate receptor 6 gene with autism. Mol. Psychiatry 7, 302-310.
71. Jamain, S., Quach, H., Betancur, C., Rastam, M., Colineaux, C., Gillberg, I. C., Soderstrom, H., Giros, B., Leboyer, M., Gillberg, C. et al.; Paris Autism Research International Sibpair Study (2003). Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat. Genet. 34, 27-29.
72. Jamieson, D. and Roberts, A. (2000). Responses of young Xenopus laevis tadpoles to light dimming: possible roles for the pineal eye. J. Exp. Biol. 203, 1857-1867.
73. Junek, S., Kludt, E., Wolf, F. and Schild, D. (2010). Olfactory coding with patterns of response latencies. Neuron 67, 872-884.
74. Kabashi, E., Brustein, E., Champagne, N. and Drapeau, P. (2011). Zebrafish models for the functional genomics of neurogenetic disorders. Biochim. Biophys. Acta 1812, 335-345.
75. Katz, L. C., Potel, M. J. and Wassersug, R. J. (1981). Structure and mechanisms of schooling in tadpoles of the clawed frog, Xenopus-Laevis. Anim. Behav. 29, 20-33.
76. Khakhalin, A. S. and Aizenman, C. D. (2012). GABAergic transmission and chloride equilibrium potential are not modulated by pyruvate in the developing optic tectum of Xenopus laevis tadpoles. PLoS ONE 7, e34446.
77. Krey, J. F. and Dolmetsch, R. E. (2007). Molecular mechanisms of autism: a possible role for Ca2+ signaling. Curr. Opin. Neurobiol. 17, 112-119.
78. Kroll, K. L. and Amaya, E. (1996). Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signaling requirements during gastrulation. Development 122, 3173-3183.
79. Landesman, Y. and Sokol, S. Y. (1997). Xwnt-2b is a novel axis-inducing Xenopus Wnt, which is expressed in embryonic brain. Mech. Dev. 63, 199-209.
80. Lee, R. H., Mills, E. A., Schwartz, N., Bell, M. R., Deeg, K. E., Ruthazer, E. S., Marsh-Armstrong, N. and Aizenman, C. D. (2010). Neurodevelopmental effects of chronic exposure to elevated levels of pro-inflammatory cytokines in a developing visual system. Neural Dev. 5, 2.
81. Levenga, J., de Vrij, F. M., Oostra, B. A. and Willemsen, R. (2010). Potential therapeutic interventions for fragile X syndrome. Trends Mol. Med. 16, 516-527.
82. Lewis, B. B., Wester, M. R., Miller, L. E., Nagarkar, M. D., Johnson, M. B. and Saha, M. S. (2009). Cloning and characterization of voltage-gated calcium channel alpha1 subunits in Xenopus laevis during development. Dev. Dyn. 238, 2891-2902.
83. Li, W. C., Roberts, A. and Soffe, S. R. (2009). Locomotor rhythm maintenance: electrical coupling among premotor excitatory interneurons in the brainstem and spinal cord of young Xenopus tadpoles. J. Physiol. 587, 1677-1693.
84. Li, J., Erisir, A. and Cline, H. (2011). In vivo time-lapse imaging and serial section electron microscopy reveal developmental synaptic rearrangements. Neuron 69, 273-286.
85. Lichtenstein, P., Carlström, E., Rastam, M., Gillberg, C. and Anckarsäter, H. (2010). The genetics of autism spectrum disorders and related neuropsychiatric disorders in childhood. Am. J. Psychiatry 167, 1357-1363.
86. Lim, J. H., Luo, T., Sargent, T. D. and Fallon, J. R. (2005). Developmental expression of Xenopus fragile X mental retardation-1 gene. Int. J. Dev. Biol. 49, 981-984.
87. Liu, X. F. and Haas, K. (2011). Single-cell electroporation in Xenopus. Cold Spring Harb. Protoc. 2011, doi: 10.1101/pdb.prot065615.
88. Liu, X. F., Tari, P. K. and Haas, K. (2009). PKM zeta restricts dendritic arbor growth by filopodial and branch stabilization within the intact and awake developing brain. J. Neurosci. 29, 12229-12235.
89. Lorenz, C., Contardo-Jara, V., Pflugmacher, S., Wiegand, C., Nützmann, G., Lutz, I. and Kloas, W. (2011). The synthetic gestagen levonorgestrel impairs metamorphosis in Xenopus laevis by disruption of the thyroid system. Toxicol. Sci. 123, 94-102.
90. Lum, A. M., Wassersug, R. J., Potel, M. J. and Lerner, S. A. (1982). Schooling behavior of tadpoles: a potential indicator of ototoxicity. Pharmacol. Biochem. Behav. 17, 363-366.
91. Marín, O. (2012). Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107-120.
92. Markram, K. and Markram, H. (2010). The intense world theory -a unifying theory of the neurobiology of autism. Front. Hum. Neurosci. 4, 224.
93. Markram, K., Rinaldi, T., La Mendola, D., Sandi, C. and Markram, H. (2008). Abnormal fear conditioning and amygdala processing in an animal model of autism. Neuropsychopharmacology 33, 901-912.
94. Marshak, S., Nikolakopoulou, A. M., Dirks, R., Martens, G. J. and Cohen-Cory, S. (2007). Cell-autonomous TrkB signaling in presynaptic retinal ganglion cells mediates axon arbor growth and synapse maturation during the establishment of retinotectal synaptic connectivity. J. Neurosci. 27, 2444-2456.
95. Marshak, S., Meynard, M. M., De Vries, Y. A., Kidane, A. H. and Cohen-Cory, S. (2012). Cell-autonomous alterations in dendritic arbor morphology and connectivity induced by overexpression of MeCP2 in Xenopus central neurons in vivo. PLoS ONE 7, e33153.
96. McKeown, C. R., Sharma, P., Sharipov, H. E., Shen, W. and Cline, H. T. (2013). Neurogenesis is required for behavioral recovery after injury in the visual system of Xenopus laevis. J. Comp. Neurol. 521, 2262-2278.
97. Miraucourt, L. S., Silva, J. S., Burgos, K., Li, J., Abe, H., Ruthazer, E. S. and Cline, H. T. (2012). GABA expression and regulation by sensory experience in the developing visual system. PLoS ONE 7, e29086.
98. Miskevich, F., Doench, J. G., Townsend, M. T., Sharp, P. A. and Constantine-Paton, M. (2006). RNA interference of Xenopus NMDAR NR1 in vitro and in vivo. J. Neurosci. Methods 152, 65-73.
99. Mu, Y. and Poo, M. M. (2006). Spike timing-dependent LTP/LTD mediates visual experience-dependent plasticity in a developing retinotectal system. Neuron 50, 115-125.
100. Nakatani, Y., Takeda, H., Kohara, Y. and Morishita, S. (2007). Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res. 17, 1254-1265.
101. Neale, B. M., Kou, Y., Liu, L., Ma'ayan, A., Samocha, K. E., Sabo, A., Lin, C. F., Stevens, C., Wang, L. S., Makarov, V. et al. (2012). Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 485, 242-245.
102. Newschaffer, C. J., Croen, L. A., Daniels, J., Giarelli, E., Grether, J. K., Levy, S. E., Mandell, D. S., Miller, L. A., Pinto-Martin, J., Reaven, J. et al. (2007). The epidemiology of autism spectrum disorders. Annu. Rev. Public Health 28, 235-258.
103. Nicholas, B., Rudrasingham, V., Nash, S., Kirov, G., Owen, M. J. and Wimpory, D. C. (2007). Association of Per1 and Npas2 with autistic disorder: support for the clock genes/social timing hypothesis. Mol. Psychiatry 12, 581-592.
104. Pai, V. P., Aw, S., Shomrat, T., Lemire, J. M. and Levin, M. (2012). Transmembrane voltage potential controls embryonic eye patterning in Xenopus laevis. Development 139, 313-323.
105. Panaitof, S. C. (2012). A songbird animal model for dissecting the genetic bases of autism spectrum disorder. Dis. Markers 33, 241-249.
106. Patterson, P. H. (2011). Modeling autistic features in animals. Pediatr. Res. 69, 34R-40R.
107. Peça, J. and Feng, G. (2012). Cellular and synaptic network defects in autism. Curr. Opin. Neurobiol. 22, 866-872.
108. Perry, W., Minassian, A., Lopez, B., Maron, L. and Lincoln, A. (2007). Sensorimotor gating deficits in adults with autism. Biol. Psychiatry 61, 482-486.
109. Podgorski, K., Dunfield, D. and Haas, K. (2012). Functional clustering drives encoding improvement in a developing brain network during awake visual learning. PLoS Biol. 10, e1001236.
110. Postlethwait, J., Amores, A., Cresko, W., Singer, A. and Yan, Y. L. (2004). Subfunction partitioning, the teleost radiation and the annotation of the human genome. Trends Genet. 20, 481-490.
111. Pratt, K. G. and Aizenman, C. D. (2007). Homeostatic regulation of intrinsic excitability and synaptic transmission in a developing visual circuit. J. Neurosci. 27, 8268-8277.
112. Pratt, K. G. and Aizenman, C. D. (2009). Multisensory integration in mesencephalic trigeminal neurons in Xenopus tadpoles. J. Neurophysiol. 102, 399-412.
113. Pratt, K. G., Dong, W. and Aizenman, C. D. (2008). Development and spike timingdependent plasticity of recurrent excitation in the Xenopus optic tectum. Nat. Neurosci. 11, 467-475.
114. Pronych, S. P., Souza, K. A., Neff, A. W. and Wassersug, R. J. (1996). Optomotor behaviour in Xenopus laevis tadpoles as a measure of the effect of gravity on visual and vestibular neural integration. J. Exp. Biol. 199, 2689-2701.
115. Rash, J. E., Kamasawa, N., Davidson, K. G., Yasumura, T., Pereda, A. E. and Nagy, J. I. (2012). Connexin composition in apposed gap junction hemiplaques revealed by matched double-replica freeze-fracture replica immunogold labeling. J. Membr. Biol. 245, 333-344.
116. Richards, S. M. and Cole, S. E. (2006). A toxicity and hazard assessment of fourteen pharmaceuticals to Xenopus laevis larvae. Ecotoxicology 15, 647-656.
117. Rinaldi, T., Silberberg, G. and Markram, H. (2008). Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid. Cereb. Cortex 18, 763-770.
118. Roberts, A., Hill, N. A. and Hicks, R. (2000). Simple mechanisms organise orientation of escape swimming in embryos and hatchling tadpoles of Xenopus laevis. J. Exp. Biol. 203, 1869-1885.
119. Root, C. M., Velázquez-Ulloa, N. A., Monsalve, G. C., Minakova, E. and Spitzer, N. C. (2008). Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. J. Neurosci. 28, 4777-4784.
120. Ruthazer, E. S., Akerman, C. J. and Cline, H. T. (2003). Control of axon branch dynamics by correlated activity in vivo. Science 301, 66-70.
121. Ruthazer, E. S., Li, J. L. and Cline, H. T. (2006). Stabilization of axon branch dynamics by synaptic maturation. J. Neurosci. 26, 3594-3603.
122. Sakaguchi, D. S., Murphey, R. K., Hunt, R. K. and Tompkins, R. (1984). The development of retinal ganglion cells in a tetraploid strain of Xenopus laevis: a morphological study utilizing intracellular dye injection. J. Comp. Neurol. 224, 231-251.
123. Samaco, R. C. and Neul, J. L. (2011). Complexities of Rett syndrome and MeCP2. J. Neurosci. 31, 7951-7959.
124. Sanes, D. H., Reh, T. A. and Harris, W. A. (2012). Development of the Nervous System. Burlington, MA: Academic Press.
125. Sharma, P. and Cline, H. T. (2010). Visual activity regulates neural progenitor cells in developing xenopus CNS through musashi1. Neuron 68, 442-455.
126. Sillar, K. T. and Robertson, R. M. (2009). Thermal activation of escape swimming in post-hatching Xenopus laevis frog larvae. J. Exp. Biol. 212, 2356-2364.
127. Simmons, A. M., Costa, L. M. and Gerstein, H. B. (2004). Lateral line-mediated rheotactic behavior in tadpoles of the African clawed frog (Xenopus laevis). J. Comp. Physiol. A 190, 747-758.
128. Spawn, A. and Aizenman, C. D. (2012). Abnormal visual processing and increased seizure susceptibility result from developmental exposure to the biocide methylisothiazolinone. Neuroscience 205, 194-204.
129. Spencer, C. M., Serysheva, E., Yuva-Paylor, L. A., Oostra, B. A., Nelson, D. L. and 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.
130. Sperry, R. W. (1963). Chemoaffinity in the orderly growth of nerve fiber patterns and connections. Proc. Natl. Acad. Sci. USA 50, 703-710.
131. Stancheva, I., Collins, A. L., Van den Veyver, I. B., Zoghbi, H. and Meehan, R. R. (2003). A mutant form of MeCP2 protein associated with human Rett syndrome cannot be displaced from methylated DNA by notch in Xenopus embryos. Mol. Cell 12, 425-435.
132. Stern, M. (2011). Insulin signaling and autism. Front Endocrinol (Lausanne) 2, 54.
133. Straka, H. (2010). Ontogenetic rules and constraints of vestibulo-ocular reflex development. Curr. Opin. Neurobiol. 20, 689-695.
134. Straka, H. and Simmers, J. (2012). Xenopus laevis: an ideal experimental model for studying the developmental dynamics of neural network assembly and sensorymotor computations. Dev. Neurobiol. 72, 649-663.
135. Takagi, C., Sakamaki, K., Morita, H., Hara, Y., Suzuki, M., Kinoshita, N. and Ueno, N. (2013). Transgenic Xenopus laevis for live imaging in cell and developmental biology. Dev. Growth Differ. 55, 422-433.
136. Tao, H. W., Zhang, L. I., Engert, F. and Poo, M. (2001). Emergence of input specificity of ltp during development of retinotectal connections in vivo. Neuron 31, 569-580.
137. Tietge, J. E., Holcombe, G. W., Flynn, K. M., Kosian, P. A., Korte, J. J., Anderson, L. E., Wolf, D. C. and Degitz, S. J. (2005). Metamorphic inhibition of Xenopus laevis by sodium perchlorate: effects on development and thyroid histology. Environ. Toxicol. Chem. 24, 926-933.
138. Tremblay, M., Fugere, V., Tsui, J., Schohl, A., Tavakoli, A., Travencolo, B. A. N., Costa, L. D. and Ruthazer, E. S. (2009). Regulation of radial glial motility by visual experience. J. Neurosci. 29, 14066-14076.
139. Tropepe, V. and Sive, H. L. (2003). Can zebrafish be used as a model to study the neurodevelopmental causes of autism? Genes Brain Behav. 2, 268-281.
140. Tsai, N. P., Wilkerson, J. R., Guo, W., Maksimova, M. A., DeMartino, G. N., Cowan, C. W. and Huber, K. M. (2012). Multiple autism-linked genes mediate synapse elimination via proteasomal degradation of a synaptic scaffold PSD-95. Cell 151, 1581-1594.
141. Tsui, J., Schwartz, N. and Ruthazer, E. S. (2010). A developmental sensitive period for spike timing-dependent plasticity in the retinotectal projection. Front. Synaptic Neurosci. 2, 13.
142. Ueno, S., Kono, R. and Iwao, Y. (2006). PTEN is required for the normal progression of gastrulation by repressing cell proliferation after MBT in Xenopus embryos. Dev. Biol. 297, 274-283.
143. Villinger, J. and Waldman, B. (2012). Social discrimination by quantitative assessment of immunogenetic similarity. Proc. Biol. Sci. 279, 4368-4374.
144. Wassersug, R. J. and Yamashita, M. (2002). Assessing and interpreting lateralised behaviours in anuran larvae. Laterality 7, 241-260.
145. Wassink, T. H., Piven, J., Vieland, V. J., Huang, J., Swiderski, R. E., Pietila, J., Braun, T., Beck, G., Folstein, S. E., Haines, J. L. et al. (2001). Evidence supporting WNT2 as an autism susceptibility gene. Am. J. Med. Genet. 105, 406-413.
146. Winlove, C. I. and Roberts, A. (2011). Pharmacology of currents underlying the different firing patterns of spinal sensory neurons and interneurons identified in vivo using multivariate analysis. J. Neurophysiol. 105, 2487-2500.
147. Wu, G., Malinow, R. and Cline, H. T. (1996). Maturation of a central glutamatergic synapse. Science 274, 972-976.
148. Xu, H., Khakhalin, A. S., Nurmikko, A. V. and Aizenman, C. D. (2011). Visual experience-dependent maturation of correlated neuronal activity patterns in a developing visual system. J. Neurosci. 31, 8025-8036.
149. Zhang, F., Degitz, S. J., Holcombe, G. W., Kosian, P. A., Tietge, J., Veldhoen, N. and Helbing, C. C. (2006). Evaluation of gene expression endpoints in the context of a Xenopus laevis metamorphosis-based bioassay to detect thyroid hormone disruptors. Aquat. Toxicol. 76, 24-36.
150. Zhuang, M. H., Wang, Y. X., Steenhard, B. M. and Besharse, J. C. (2000). Differential regulation of two period genes in the Xenopus eye. Brain Res. Mol. Brain Res. 82, 52-64.
151. Zoeller, R. T. and Crofton, K. M. (2000). Thyroid hormone action in fetal brain development and potential for disruption by environmental chemicals. Neurotoxicology 21, 935-945.