Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2012 (2012), Article ID 275630, 12 pages
http://dx.doi.org/10.1155/2012/275630
Review Article

Pathological Plasticity in Fragile X Syndrome

1Center for Neuroscience Research, Children's National Medical Center, Washington, DC 20010, USA
2Interdisciplinary Program in Neuroscience, Georgetown University Medical Center, Washington, DC 20057, USA

Received 9 March 2012; Accepted 21 May 2012

Academic Editor: Laurie C. Doering

Copyright © 2012 Brandon S. Martin and Molly M. Huntsman. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. B. A. de Vries, D. J. J. Halley, B. A. Oostra, and M. F. Niermeijer, “The fragile X syndrome,” Journal of Medical Genetics, vol. 35, no. 7, pp. 579–589, 1998. View at Google Scholar · View at Scopus
  2. R. J. Hagerman, E. Berry-Kravis, W. E. Kaufmann et al., “Advances in the treatment of fragile x Syndrome,” Pediatrics, vol. 123, no. 1, pp. 378–390, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. M. R. Tranfaglia, “The psychiatric presentation of fragile x: evolution of the diagnosis and treatment of the psychiatric comorbidities of fragile X syndrome,” Developmental Neuroscience, vol. 33, no. 5, pp. 337–348, 2011. View at Publisher · View at Google Scholar
  4. A. J. M. H. Verkerk, M. Pieretti, J. S. Sutcliffe et al., “Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome,” Cell, vol. 65, no. 5, pp. 905–914, 1991. View at Google Scholar · View at Scopus
  5. Y. H. Fu, D. P. A. Kuhl, A. Pizzuti et al., “Variation of the CGG repeat at the fragile X site results in genetic instability: resolution of the sherman paradox,” Cell, vol. 67, no. 6, pp. 1047–1058, 1991. View at Google Scholar · View at Scopus
  6. H. Wang, L. Ku, D. J. Osterhout et al., “Developmentally-programmed FMRP expression in oligodendrocytes: a potential role of FMRP in regulating translation in oligodendroglia progenitors,” Human Molecular Genetics, vol. 13, no. 1, pp. 79–89, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. J. L. Olmos-Serrano, S. M. Paluszkiewicz, B. S. Martin, W. E. Kaufmann, J. G. Corbin, and M. M. Huntsman, “Defective GABAergic neurotransmission and pharmacological rescue of neuronal hyperexcitability in the amygdala in a mouse model of fragile X syndrome,” Journal of Neuroscience, vol. 30, no. 29, pp. 9929–9938, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Devys, Y. Lutz, N. Rouyer, J. P. Bellocq, and J. L. Mandel, “The FMR-1 protein is cytoplasmic, most abundant in neurons and appears normal in carriers of a fragile X premutation,” Nature Genetics, vol. 4, no. 4, pp. 335–340, 1993. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. Feng, D. Absher, D. E. Eberhart, V. Brown, H. E. Malter, and S. T. Warren, “FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association,” Molecular Cell, vol. 1, no. 1, pp. 109–118, 1997. View at Google Scholar · View at Scopus
  10. H. L. Hinds, C. T. Ashley, J. S. Sutcliffe et al., “Tissue specific expression of FMR-1 provides evidence for a functional role in fragile X syndrome,” Nature Genetics, vol. 3, no. 1, pp. 36–43, 1993. View at Publisher · View at Google Scholar · View at Scopus
  11. L. N. Antar, C. Li, H. Zhang, R. C. Carroll, and G. J. Bassell, “Local functions for FMRP in axon growth cone motility and activity-dependent regulation of filopodia and spine synapses,” Molecular and Cellular Neuroscience, vol. 32, no. 1-2, pp. 37–48, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. Z. Li, Y. Zhang, L. Ku, K. D. Wilkinson, S. T. Warren, and Y. Feng, “The fragile X mental retardation protein inhibits translation via interacting with mRNA,” Nucleic Acids Research, vol. 29, no. 11, pp. 2276–2283, 2001. View at Google Scholar · View at Scopus
  13. S. B. Christie, M. R. Akins, J. E. Schwob, and J. R. Fallon, “The FXG: a presynaptic Fragile X granule expressed in a subset of developing brain circuits,” Journal of Neuroscience, vol. 29, no. 5, pp. 1514–1524, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Laggerbauer, D. Ostareck, E. M. Keidel, A. Ostareck-Lederer, and U. Fischer, “Evidence that fragile X mental retardation protein is a negative regulator of translation,” Human Molecular Genetics, vol. 10, no. 4, pp. 329–338, 2001. View at Google Scholar · View at Scopus
  15. K. M. Huber, S. M. Gallagher, S. T. Warren, and M. F. Bear, “Altered synaptic plasticity in a mouse model of fragile X mental retardation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 11, pp. 7746–7750, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. V. Brown, P. Jin, S. Ceman et al., “Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome,” Cell, vol. 107, no. 4, pp. 477–487, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. J. C. Darnell, O. Mostovetsky, and R. B. Darnell, “FMRP RNA targets: identification and validation,” Genes, Brain and Behavior, vol. 4, no. 6, pp. 341–349, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. J. C. Darnell, S. J. Van Driesche, C. Zhang et al., “FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism,” Cell, vol. 146, no. 2, pp. 247–261, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. G. J. Bassell and S. T. Warren, “Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function,” Neuron, vol. 60, no. 2, pp. 201–214, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Berry-Kravis, “Epilepsy in fragile X syndrome,” Developmental Medicine and Child Neurology, vol. 44, no. 11, pp. 724–728, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. P. J. Hagerman and C. E. Stafstrom, “Origins of epilepsy in fragile X syndrome,” Epilepsy Currents, vol. 9, no. 4, pp. 108–112, 2009. View at Publisher · View at Google Scholar
  22. L. J. Miller, D. N. McIntosh, J. McGrath et al., “Electrodermal responses to sensory stimuli in individuals with fragile X syndrome: a preliminary report,” American Journal of Medical Genetics, vol. 83, no. 4, pp. 268–279, 1999. View at Publisher · View at Google Scholar
  23. S. A. Musumeci, R. J. Hagerman, R. Ferri et al., “Epilepsy and EEG findings in males with fragile X syndrome,” Epilepsia, vol. 40, no. 8, pp. 1092–1099, 1999. View at Publisher · View at Google Scholar · View at Scopus
  24. W. Chonchaiya, A. Schneider, and R. J. Hagerman, “Fragile X: a family of disorders,” Advances in Pediatrics, vol. 56, no. 1, pp. 165–186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. C. E. Bakker, C. Verheij, R. Willemsen et al., “Fmr1 knockout mice: a model to study fragile X mental retardation,” Cell, vol. 78, no. 1, pp. 23–33, 1994. View at Google Scholar · View at Scopus
  26. G. Dölen, E. Osterweil, B. S. S. Rao et al., “Correction of fragile X syndrome in mice,” Neuron, vol. 56, no. 6, pp. 955–962, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. S. A. Musumeci, G. Calabrese, C. M. Bonaccorso et al., “Audiogenic seizure susceptibility is reduced in fragile X knockout mice after introduction of FMR1 transgenes,” Experimental Neurology, vol. 203, no. 1, pp. 233–240, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. T. A. Comery, J. B. Harris, P. J. Willems et al., “Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 10, pp. 5401–5404, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. V. J. Hinton, W. T. Brown, K. Wisniewski, and R. D. Rudelli, “Analysis of neocortex in three males with the fragile X syndrome,” American Journal of Medical Genetics, vol. 41, no. 3, pp. 289–294, 1991. View at Google Scholar · View at Scopus
  30. S. A. Irwin, R. Galvez, and W. T. Greenough, “Dendritic spine structural anomalies in fragile-X mental retardation syndrome,” Cerebral Cortex, vol. 10, no. 10, pp. 1038–1044, 2000. View at Google Scholar · View at Scopus
  31. M. F. Bear, K. M. Huber, and S. T. Warren, “The mGluR theory of fragile X mental retardation,” Trends in Neurosciences, vol. 27, no. 7, pp. 370–377, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Pan and K. S. Broadie, “Drosophila fragile X mental retardation protein and metabotropic glutamate receptor a convergently regulate the synaptic ratio of ionotropic glutamate receptor subclasses,” Journal of Neuroscience, vol. 27, no. 45, pp. 12378–12389, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Pan, E. Woodruff, P. Liang, and K. Broadie, “Mechanistic relationships between Drosophila fragile X mental retardation protein and metabotropic glutamate receptor A signaling,” Molecular and Cellular Neuroscience, vol. 37, no. 4, pp. 747–760, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Repicky and K. Broadie, “Metabotropic glutamate receptor-mediated use-dependent down-regulation of synaptic excitability involves the fragile X mental retardation protein,” Journal of Neurophysiology, vol. 101, no. 2, pp. 672–687, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. F. Gasparini, K. Lingenhöhl, N. Stoehr et al., “2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist,” Neuropharmacology, vol. 38, no. 10, pp. 1493–1503, 1999. View at Publisher · View at Google Scholar · View at Scopus
  36. Q. J. Yan, M. Rammal, M. Tranfaglia, and R. P. Bauchwitz, “Suppression of two major fragile X Syndrome mouse model phenotypes by the mGluR5 antagonist MPEP,” Neuropharmacology, vol. 49, no. 7, pp. 1053–1066, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. F. M. S. de Vrij, J. Levenga, H. C. van der Linde et al., “Rescue of behavioral phenotype and neuronal protrusion morphology in Fmr1 KO mice,” Neurobiology of Disease, vol. 31, no. 1, pp. 127–132, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Aschrafi, B. A. Cunningham, G. M. Edelman, and P. W. Vanderklish, “The fragile X mental retardation protein and group I metabotropic glutamate receptors regulate levels of mRNA granules in brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 6, pp. 2180–2185, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. S. M. J. McBride, C. H. Choi, Y. Wang et al., “Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of Fragile X syndrome,” Neuron, vol. 45, no. 5, pp. 753–764, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Michalon, M. Sidorov, T. M. Ballard et al., “Chronic pharmacological mGlu5 inhibition corrects fragile X in adult mice,” Neuron, vol. 74, no. 1, pp. 49–56, 2012. View at Publisher · View at Google Scholar
  41. I. J. Weiler, S. A. Irwin, A. Y. Klintsova et al., “Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 10, pp. 5395–5400, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. K. M. Huber, M. S. Kayser, and M. F. Bear, “Role for rapid dendritic protein synthesis in hippocampal mGluR- dependent long-term depression,” Science, vol. 288, no. 5469, pp. 1254–1256, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. I. J. Weiler, C. C. Spangler, A. Y. Klintsova et al., “Fragile X mental retardation protein is necessary for neurotransmitter- activated protein translation at synapses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 50, pp. 17504–17509, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. S. K. E. Koekkoek, K. Yamaguchi, B. A. Milojkovic et al., “Deletion of FMR1 in purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in fragile X syndrome,” Neuron, vol. 47, no. 3, pp. 339–352, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. J. M. Godfraind, E. Reyniers, K. De Boulle et al., “Long-term potentiation in the hippocampus of fragile X knockout mice,” American Journal of Medical Genetics, vol. 64, no. 2, pp. 246–251, 1996. View at Publisher · View at Google Scholar
  46. W. Paradee, H. E. Melikian, D. L. Rasmussen, A. Kenneson, P. J. Conn, and S. T. Warren, “Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function,” Neuroscience, vol. 94, no. 1, pp. 185–192, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Li, M. R. Pelletier, J. L. Perez Velazquez, and P. L. Carlen, “Reduced cortical synaptic plasticity and GluR1 expression associated with fragile X mental retardation protein deficiency,” Molecular and Cellular Neuroscience, vol. 19, no. 2, pp. 138–151, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. B. M. Wilson and C. L. Cox, “Absence of metabotropic glutamate receptor-mediated plasticity in the neocortex of fragile X mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 7, pp. 2454–2459, 2007. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Suvrathan, C. A. Hoeffer, H. Wong, E. Klann, and S. Chattarji, “Characterization and reversal of synaptic defects in the amygdala in a mouse model of fragile X syndrome,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 25, pp. 11591–11596, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. M.-G. Zhao, H. Toyoda, S. W. Ko, H. K. Ding, L. J. Wu, and M. Zhuo, “Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome,” Journal of Neuroscience, vol. 25, no. 32, pp. 7385–7392, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. H. Y. Lee, W. P. Ge, W. Huang et al., “Bidirectional regulation of dendritic voltage-gated potassium channels by the fragile X mental retardation protein,” Neuron, vol. 72, no. 4, pp. 630–642, 2011. View at Publisher · View at Google Scholar
  52. S. M. Till, H. L. Li, M. C. Miniaci, E. R. Kandel, and Y. B. Choi, “A presynaptic role for FMRP during protein synthesis-dependent long-term plasticity in Aplysia,” Learning and Memory, vol. 18, no. 1, pp. 39–48, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. P. Y. Deng, D. Sojka, and V. A. Klyachko, “Abnormal presynaptic short-term plasticity and information processing in a mouse model of fragile X syndrome,” Journal of Neuroscience, vol. 31, no. 30, pp. 10971–10982, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Bacci, J. R. Huguenard, and D. A. Prince, “Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids,” Nature, vol. 431, no. 7006, pp. 312–316, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. R. I. Wilson and R. A. Nicoll, “Neuroscience: endocannabinoid signaling in the brain,” Science, vol. 296, no. 5568, pp. 678–682, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. U. Misgeld, M. Bijak, and W. Jarolimek, “A physiological role for GABA(B) receptors and the effects of baclofen in the mammalian central nervous system,” Progress in Neurobiology, vol. 46, no. 4, pp. 423–462, 1995. View at Publisher · View at Google Scholar · View at Scopus
  57. N. Varma, G. C. Carlson, C. Ledent, and B. E. Alger, “Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus,” The Journal of Neuroscience, vol. 21, no. 24, p. RC188, 2001. View at Google Scholar · View at Scopus
  58. J. R. Gibson, A. F. Bartley, S. A. Hays, and K. M. Huber, “Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome,” Journal of Neurophysiology, vol. 100, no. 5, pp. 2615–2626, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. L. Zhang and B. E. Alger, “Enhanced endocannabinoid signaling elevates neuronal excitability in fragile X syndrome,” Journal of Neuroscience, vol. 30, no. 16, pp. 5724–5729, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. S.-H. Lee, C. Földy, and I. Soltesz, “Distinct endocannabinoid control of GABA release at perisomatic and dendritic synapses in the hippocampus,” Journal of Neuroscience, vol. 30, no. 23, pp. 7993–8000, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Trettel and E. S. Levine, “Cannabinoids depress inhibitory synaptic inputs received by layer 2/3 pyramidal neurons of the neocortex,” Journal of Neurophysiology, vol. 88, no. 1, pp. 534–539, 2002. View at Google Scholar · View at Scopus
  62. A. Bacci, J. R. Huguenard, and D. A. Prince, “Modulation of neocortical interneurons: extrinsic influences and exercises in self-control,” Trends in Neurosciences, vol. 28, no. 11, pp. 602–610, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. E. E. Fanselow, K. A. Richardson, and B. W. Connors, “Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex,” Journal of Neurophysiology, vol. 100, no. 5, pp. 2640–2652, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. M. Beierlein, J. R. Gibson, and B. W. Connors, “A network of electrically coupled interneurons drives synchronized inhibition in neocortex,” Nature Neuroscience, vol. 3, no. 9, pp. 904–910, 2000. View at Publisher · View at Google Scholar · View at Scopus
  65. S. M. Paluszkiewicz, J. L. Olmos-Serrano, J. G. Corbin, and M. M. Huntsman, “Impaired inhibitory control of cortical synchronization in fragile X syndrome,” J Neurophysiol, vol. 106, no. 5, pp. 2264–2272, 2011. View at Publisher · View at Google Scholar
  66. E. E. Fanselow and B. W. Connors, “The roles of somatostatin-expressing (GIN) and fast-spiking inhibitory interneurons in up-down states of mouse neocortex,” Journal of Neurophysiology, vol. 104, no. 2, pp. 596–606, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. M. A. Long, S. J. Cruikshank, M. J. Jutras, and B. W. Connors, “Abrupt maturation of a spike-synchronizing mechanism in neocortex,” Journal of Neuroscience, vol. 25, no. 32, pp. 7309–7316, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. L. R. Merlin and R. K. S. Wong, “Role of group I metabotropic glutamate receptors in the patterning of epileptiform activities in vitro,” Journal of Neurophysiology, vol. 78, no. 1, pp. 539–544, 1997. View at Google Scholar · View at Scopus
  69. L. R. Merlin, P. J. Bergold, and R. K. S. Wong, “Requirement of protein synthesis for group I mGluR-mediated induction of epileptiform discharges,” Journal of Neurophysiology, vol. 80, no. 2, pp. 989–993, 1998. View at Google Scholar · View at Scopus
  70. J. P. Lieb, J. Engel, and W. J. Brown, “Neuropathological findings following temporal lobectomy related to surface and deep EEG patterns,” Epilepsia, vol. 22, no. 5, pp. 539–549, 1981. View at Google Scholar · View at Scopus
  71. G. W. Taylor, L. R. Merlin, and R. K. S. Wong, “Synchronized oscillations in hippocampal CA3 neurons induced by metabotropic glutamate receptor activation,” Journal of Neuroscience, vol. 15, no. 12, pp. 8039–8052, 1995. View at Google Scholar · View at Scopus
  72. W. Zhao, R. Bianchi, M. Wang, and R. K. S. Wong, “Extracellular signal-regulated kinase 1/2 is required for the induction of group I metabotropic glutamate receptor-mediated epileptiform discharges,” Journal of Neuroscience, vol. 24, no. 1, pp. 76–84, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. A. C. Lee, R. K. S. Wong, S. C. Chuang, H. S. Shin, and R. Bianchi, “Role of synaptic metabotropic glutamate receptors in epileptiform discharges in hippocampal slices,” Journal of Neurophysiology, vol. 88, no. 4, pp. 1625–1633, 2002. View at Google Scholar · View at Scopus
  74. R. Bianchi, S. C. Chuang, W. Zhao, S. R. Young, and R. K. S. Wong, “Cellular plasticity for group I mGluR-mediated epileptogenesis,” Journal of Neuroscience, vol. 29, no. 11, pp. 3497–3507, 2009. View at Publisher · View at Google Scholar · View at Scopus
  75. R. K. S. Wong, S. C. Chuang, and R. Bianchi, “Plasticity mechanisms underlying mGluR-induced epileptogenesis,” Advances in Experimental Medicine and Biology, vol. 548, pp. 69–75, 2004. View at Google Scholar · View at Scopus
  76. S. C. Chuang, R. Bianchi, and R. K. S. Wong, “Group I mGluR activation turns on a voltage-gated inward current in hippocampal pyramidal cells,” Journal of Neurophysiology, vol. 83, no. 5, pp. 2844–2853, 2000. View at Google Scholar · View at Scopus
  77. S. C. Chuang, R. Bianchi, D. Kim, H. S. Shin, and R. K. S. Wong, “Group I metabotropic glutamate receptors elicit epileptiform discharges in the hippocampus through PLCβ1 signaling,” Journal of Neuroscience, vol. 21, no. 16, pp. 6387–6394, 2001. View at Google Scholar · View at Scopus
  78. Y. Shang, H. Wang, V. Mercaldo, X. Li, T. Chen, and M. Zhuo, “Fragile X mental retardation protein is required for chemically-induced long-term potentiation of the hippocampus in adult mice,” Journal of Neurochemistry, vol. 111, no. 3, pp. 635–646, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. S.-C. Chuang, W. Zhao, R. Bauchwitz, Q. Yan, R. Bianchi, and R. K. S. Wong, “Prolonged epileptiform discharges induced by altered group I metabotropic glutamate receptor-mediated synaptic responses in hippocampal slices of a fragile X mouse model,” Journal of Neuroscience, vol. 25, no. 35, pp. 8048–8055, 2005. View at Publisher · View at Google Scholar · View at Scopus
  80. J. Zhong, S. C. Chuang, R. Bianchi et al., “BC1 regulation of metabotropic glutamate receptor-mediated neuronal excitability,” Journal of Neuroscience, vol. 29, no. 32, pp. 9977–9986, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. J. Zhong, S. C. Chuang, R. Bianchi et al., “Regulatory BC1 RNA and the fragile X mental retardation protein: convergent functionality in brain,” PLoS ONE, vol. 5, no. 11, Article ID e15509, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. R. Dahlhaus and A. El-Husseini, “Altered neuroligin expression is involved in social deficits in a mouse model of the fragile X syndrome,” Behavioural brain research, vol. 208, no. 1, pp. 96–105, 2010. View at Google Scholar · View at Scopus
  83. G. Curia, T. Papouin, P. Séguéla, and M. Avoli, “Downregulation of tonic GABAergic inhibition in a mouse model of fragile X syndrome,” Cerebral Cortex, vol. 19, no. 7, pp. 1515–1520, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. G. G. Turrigiano and S. B. Nelson, “Homeostatic plasticity in the developing nervous system,” Nature Reviews Neuroscience, vol. 5, no. 2, pp. 97–107, 2004. View at Google Scholar · View at Scopus
  85. G. W. Davis, “Homeostatic control of neural activity: from phenomenology to molecular design,” Annual Review of Neuroscience, vol. 29, pp. 307–323, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. B. Maghsoodi, M. M. Poon, C. I. Nam, J. Aoto, P. Ting, and L. Chen, “Retinoic acid regulates RARα-mediated control of translation in dendritic RNA granules during homeostatic synaptic plasticity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 41, pp. 16015–16020, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Aoto, C. I. Nam, M. M. Poon, P. Ting, and L. Chen, “Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity,” Neuron, vol. 60, no. 2, pp. 308–320, 2008. View at Publisher · View at Google Scholar · View at Scopus
  88. M. E. Soden and L. Chen, “Fragile X protein FMRP is required for homeostatic plasticity and regulation of synaptic strength by retinoic acid,” Journal of Neuroscience, vol. 30, no. 50, pp. 16910–16921, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. J. J. LeBlanc and M. Fagiolini, “Autism: a “critical period” disorder?” Neural Plasticity, vol. 2011, Article ID 921680, 17 pages, 2011. View at Publisher · View at Google Scholar
  90. T. K. Hensch, “Critical period regulation,” Annual Review of Neuroscience, vol. 27, pp. 549–579, 2004. View at Publisher · View at Google Scholar · View at Scopus
  91. D. H. Hubel and T. N. Wiesel, “The period of susceptibility to the physiological effects of unilateral eye closure in kittens,” Journal of Physiology, vol. 206, no. 2, pp. 419–436, 1970. View at Google Scholar · View at Scopus
  92. R. V. Harrison, K. A. Gordon, and R. J. Mount, “Is there a critical period for cochlear implantation in congenitally deaf children? Analyses of hearing and speech perception performance after implantation,” Developmental Psychobiology, vol. 46, no. 3, pp. 252–261, 2005. View at Publisher · View at Google Scholar · View at Scopus
  93. M. V. Popescu and D. B. Polley, “Monaural deprivation disrupts development of binaural selectivity in auditory midbrain and cortex,” Neuron, vol. 65, no. 5, pp. 718–731, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. K. Fox, “A critical period for experience-dependent synaptic plasticity in rat barrel cortex,” Journal of Neuroscience, vol. 12, no. 5, pp. 1826–1838, 1992. View at Google Scholar · View at Scopus
  95. H. Van Der Loos and T. A. Woolsey, “Somatosensory cortex: structural alterations following early injury to sense organs,” Science, vol. 179, no. 4071, pp. 395–398, 1973. View at Google Scholar · View at Scopus
  96. M. S. Banks, R. N. Aslin, and R. D. Letson, “Sensitive period for the development of human binocular vision,” Science, vol. 190, no. 4215, pp. 675–677, 1975. View at Google Scholar · View at Scopus
  97. N. Berardi, T. Pizzorusso, and L. Maffei, “Critical periods during sensory development,” Current Opinion in Neurobiology, vol. 10, no. 1, pp. 138–145, 2000. View at Publisher · View at Google Scholar · View at Scopus
  98. G. T. Baranek, J. E. Roberts, F. J. David et al., “Developmental trajectories and correlates of sensory processing in young boys with fragile X syndrome,” Physical and Occupational Therapy in Pediatrics, vol. 28, no. 1, pp. 79–98, 2008. View at Publisher · View at Google Scholar · View at Scopus
  99. S. J. Rogers, S. Hepburn, and E. Wehner, “Parent reports of sensory symptoms in toddlers with autism and those with other developmental disorders,” Journal of Autism and Developmental Disorders, vol. 33, no. 6, pp. 631–642, 2003. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Abitbol, C. Menini, A. L. Delezoide, T. Rhyner, M. Vekemans, and J. Mallet, “Nucleus basalis magnocellularis and hippocampus are the major sites of FMR-1 expression in the human fetal brain,” Nature Genetics, vol. 4, no. 2, pp. 147–153, 1993. View at Publisher · View at Google Scholar · View at Scopus
  101. C. Agulhon, P. Blanchet, A. Kobetz et al., “Expression of FMR1, FXR1, and FXR2 genes in human prenatal tissues,” Journal of Neuropathology & Experimental Neurology, vol. 58, no. 8, pp. 867–880, 1999. View at Publisher · View at Google Scholar
  102. F. Tamanini, R. Willemsen, L. Van Unen et al., “Differential expression of FMR1, FXR1 and FXR2 proteins in human brain and testis,” Human Molecular Genetics, vol. 6, no. 8, pp. 1315–1322, 1997. View at Publisher · View at Google Scholar · View at Scopus
  103. E. G. Harlow, S. M. Till, T. A. Russell, L. S. Wijetunge, P. Kind, and A. Contractor, “Critical period plasticity is disrupted in the barrel cortex of Fmr1 knockout mice,” Neuron, vol. 65, no. 3, pp. 385–398, 2010. View at Publisher · View at Google Scholar · View at Scopus
  104. P. K. Todd, J. S. Malter, and K. J. Mack, “Whisker stimulation-dependent translation of FMRP in the barrel cortex requires activation of type I metabotropic glutamate receptors,” Molecular Brain Research, vol. 110, no. 2, pp. 267–278, 2003. View at Publisher · View at Google Scholar · View at Scopus
  105. K. Boer, F. Encha-Razavi, M. Sinico, and E. Aronica, “Differential distribution of group I metabotropic glutamate receptors in developing human cortex,” Brain Research C, vol. 1324, pp. 24–33, 2010. View at Publisher · View at Google Scholar · View at Scopus
  106. M. V. Catania, G. B. Landwehrmeyer, C. M. Testa, D. G. Standaert, J. B. Penney, and A. B. Young, “Metabotropic glutamate receptors are differentially regulated during development,” Neuroscience, vol. 61, no. 3, pp. 481–495, 1994. View at Publisher · View at Google Scholar
  107. M. Castiglione, M. Calafiore, L. Costa, M. A. Sortino, F. Nicoletti, and A. Copani, “Group I metabotropic glutamate receptors control proliferation, survival and differentiation of cultured neural progenitor cells isolated from the subventricular zone of adult mice,” Neuropharmacology, vol. 55, no. 4, pp. 560–567, 2008. View at Publisher · View at Google Scholar · View at Scopus
  108. V. Di Giorgi-Gerevini, D. Melchiorri, G. Battaglia et al., “Endogenous activation of metabotropic glutamate receptors supports the proliferation and survival of neural progenitor cells,” Cell Death and Differentiation, vol. 12, no. 8, pp. 1124–1133, 2005. View at Publisher · View at Google Scholar · View at Scopus
  109. G. López-Bendito, R. Shigemoto, A. Fairén, and R. Luján, “Differential distribution of group I metabotropic glutamate receptors during rat cortical development,” Cerebral Cortex, vol. 12, no. 6, pp. 625–638, 2002. View at Google Scholar · View at Scopus
  110. S. M. Paluszkiewicz, B. S. Martin, and M. M. Huntsman, “Fragile X syndrome: the GABAergic system and circuit dysfunction,” Developmental Neuroscience, vol. 33, no. 5, pp. 349–364, 2011. View at Publisher · View at Google Scholar
  111. D. C. Adusei, L. K. K. Pacey, D. Chen, and D. R. Hampson, “Early developmental alterations in GABAergic protein expression in fragile X knockout mice,” Neuropharmacology, vol. 59, no. 3, pp. 167–171, 2010. View at Publisher · View at Google Scholar · View at Scopus
  112. C. D'Hulst, N. De Geest, S. P. Reeve et al., “Decreased expression of the GABAA receptor in fragile X syndrome,” Brain Research, vol. 1121, no. 1, pp. 238–245, 2006. View at Publisher · View at Google Scholar · View at Scopus
  113. C. D'Hulst, I. Heulens, J. R. Brouwer et al., “Expression of the GABAergic system in animal models for fragile X syndrome and fragile X associated tremor/ataxia syndrome (FXTAS),” Brain Research C, vol. 1253, pp. 176–183, 2009. View at Publisher · View at Google Scholar · View at Scopus
  114. I. Gantois, J. Vandesompele, F. Speleman et al., “Expression profiling suggests underexpression of the GABA(A) receptor subunit delta in the fragile X knockout mouse model,” Neurobiology of Disease, vol. 21, no. 2, pp. 346–357, 2006. View at Publisher · View at Google Scholar
  115. M. Fagiolini, H. Katagiri, H. Miyamoto et al., “Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 5, pp. 2854–2859, 2003. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Fagiolini, J. M. Fritschy, K. Löw, H. Möhler, U. Rudolph, and T. K. Hensch, “Specific GABAA circuits for visual cortical plasticity,” Science, vol. 303, no. 5664, pp. 1681–1683, 2004. View at Publisher · View at Google Scholar · View at Scopus
  117. T. K. Hensch, M. Fagiolini, N. Mataga, M. P. Stryker, S. Baekkeskov, and S. F. Kash, “Local GABA circuit control of experience-dependent plasticity in developing visual cortex,” Science, vol. 282, no. 5393, pp. 1504–1508, 1998. View at Google Scholar · View at Scopus
  118. M. Y. Frenkel and M. F. Bear, “How monocular deprivation shifts ocular dominance in visual cortex of young mice,” Neuron, vol. 44, no. 6, pp. 917–923, 2004. View at Publisher · View at Google Scholar · View at Scopus
  119. T. A. Woolsey and H. Van der Loos, “The structural organization of layer IV in the somatosensory region (S I) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units,” Brain Research, vol. 17, no. 2, pp. 205–242, 1970. View at Google Scholar · View at Scopus
  120. S. M. Till, L. S. Wijetunge, V. G. Seidel et al., “Altered maturation of the primary somatosensory cortex in a mouse model of fragile X syndrome,” Human Molecular Genetics, vol. 21, no. 10, pp. 2143–2156, 2012. View at Publisher · View at Google Scholar
  121. A. Cruz-Martín, M. Crespo, and C. Portera-Cailliau, “Delayed stabilization of dendritic spines in fragile X mice,” Journal of Neuroscience, vol. 30, no. 23, pp. 7793–7803, 2010. View at Publisher · View at Google Scholar · View at Scopus
  122. J. B. Dictenberg, S. A. Swanger, L. N. Antar, R. H. Singer, and G. J. Bassell, “A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome,” Developmental Cell, vol. 14, no. 6, pp. 926–939, 2008. View at Publisher · View at Google Scholar · View at Scopus
  123. I. Bureau, G. M. G. Shepherd, and K. Svoboda, “Circuit and plasticity defects in the developing somatosensory cortex of Fmr1 knock-out mice,” Journal of Neuroscience, vol. 28, no. 20, pp. 5178–5188, 2008. View at Publisher · View at Google Scholar · View at Scopus
  124. L. Chen and M. Toth, “Fragile X mice develop sensory hyperreactivity to auditory stimuli,” Neuroscience, vol. 103, no. 4, pp. 1043–1050, 2001. View at Publisher · View at Google Scholar · View at Scopus
  125. D. D. Krueger and M. F. Bear, “Toward fulfilling the promise of molecular medicine in fragile X syndrome,” Annual Review of Medicine, vol. 62, pp. 411–429, 2011. View at Publisher · View at Google Scholar · View at Scopus
  126. P. J. Zhu and D. M. Lovinger, “Developmental alteration of endocannabinoid retrograde signaling in the hippocampus,” Journal of Neurophysiology, vol. 103, no. 2, pp. 1123–1129, 2010. View at Publisher · View at Google Scholar · View at Scopus
  127. G. G. Turrigiano and S. B. Nelson, “Hebb and homeostasis in neuronal plasticity,” Current Opinion in Neurobiology, vol. 10, no. 3, pp. 358–364, 2000. View at Publisher · View at Google Scholar · View at Scopus
  128. Z. J. Huang, A. Kirkwood, T. Pizzorusso et al., “BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex,” Cell, vol. 98, no. 6, pp. 739–755, 1999. View at Publisher · View at Google Scholar · View at Scopus
  129. S. Sugiyama, A. A. Di Nardo, S. Aizawa et al., “Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity,” Cell, vol. 134, no. 3, pp. 508–520, 2008. View at Publisher · View at Google Scholar · View at Scopus
  130. S. A. Hays, K. M. Huber, and J. R. Gibson, “Altered neocortical rhythmic activity states in Fmr1 KO mice are due to enhanced mGluR5 signaling and involve changes in excitatory circuitry,” Journal of Neuroscience, vol. 31, no. 40, pp. 14223–14234, 2011. View at Publisher · View at Google Scholar
  131. R. L. Vislay-Meltzer, S. Kratovac, L. Olmos-Serrano et al., “The development and consequences of inhibitory deficits in the fragile X amygdala,” in Proceedings of the 41st Annual Society For Neuroscience Meeting, Washington, DC, USA, 2011, Poster#774.02/O12.