Early postnatal plasticity in neocortex of Fmr1 knockout mice

Journal of Neurophysiology

Volumn 96, Issue 4, 2006, Pages 1734-1745

  Desai, Niraj S ^a,c   Casimiro, Tanya M ^a   Gruber, Stephen M ^a   Vanderklish, Peter W ^b  

^a NEUROSCIENCES INSTITUTE   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c Neurosciences Fine Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; GLUTAMATE RECEPTOR 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; ENZYME ACTIVATION; KNOCKOUT MOUSE; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOUSE; NEOCORTEX; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SYNAPSE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOCORTEX; NEURONAL PLASTICITY; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33749517734     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00221.2006     Document Type: Article

References (83)

1. Abbott LF and Nelson SB. Synaptic plasticity: taming the beast. Nat Neurosci 3: 1178-1183, 2001.
2. Abraham WC, Mason-Parker SE, Bear MF, Webb S, and Tate WP. Heterosynaptic metaplasticity in the hippocampus in vivo: a BCM-like modifiable threshold for LTP. Proc Natl Acad Sci USA 98: 10924-10929, 2001.
3. Antar LN, Afroz R, Dictenberg JB, Carroll RC, and Bassell GJ. Metabotropic glutamate receptor activation regulates fragile x mental retardation protein and Fmr1 mRNA localization differentially in dendrites and at synapses. J Neurosci 24: 2648-2655, 2004.
4. Anwyl R. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 29: 83-120, 1999.
5. Aschrafi A, Cunningham BA, Edelman GM, and Vanderklish PW. The fragile X mental retardation protein and group I metabotropic glutamate receptors regulate levels of mRNA granules in brain. Proc Natl Acad Sci USA 102: 2180-2185, 2005.
6. Bagni C and Greenough WT. From mRNP trafficking to spine dysmorphogenesis: the roots of Fragile X syndrome. Nat Rev Neurosci 6: 376-386, 2005.
7. Bear MF. Therapeutic implications of the mGluR theory of Fragile X mental retardation. Genes Brain Behav 4: 393-398, 2005.
8. Bear MF, Huber KM, and Warren ST. The mGluR theory of Fragile X mental retardation. Trends Neurosc 27: 370-377, 2004.
9. Bender VA, Bender KJ, Brasier DJ, and Feldman DE. Two coincidence detectors for spike timing-dependent plasticity in somatosensory cortex. J Neurosci 26: 4166-4177, 2006.
10. Bloodgood BL and Sabatini BL. Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310: 866-869, 2005.
11. Blue ME, Martin LJ, Brennan EM, and Johnson MV. Ontogeny of non-NMDA glutamate receptors in rat barrel cortex: I. Metabotropic receptors. J Comp Neurol 386: 16-28, 1997.
12. Blue ME and Parnavelas JG. The formation and maturation of synapses in the visual cortex of the rat. I. Quantitative analysis. J Neurocytol 12: 599-616, 1983.
13. Calverley RK and Jones DG. Contributions of dendritic spines and perforated synapses to synaptic plasticity. Brain Res Brain Res Rev 15: 215-249, 1990.
14. Carandini M and Ferster D. Membrane potential and firing rate in cat primary visual cortex. J Neurosci 20: 470-484, 2000.
15. Celikel T, Szostak VA, and Feldman DE. Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat Neurosci 7:534 -541, 2004.
16. Chevaleyre V, Takahashi KA, and Castillo PE. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu Rev Neurosci 18: 37-75, 2006.
17. Chuang SC, Zhao W, Bauchwitz R, Yan Q, Bianchi R, and Wong RKS. Prolonged epileptiform discharges induced by altered group I metabotropic glutamate receptor-mediated synaptic responses in hippocampal slices of a Fragile X mouse model. J Neurosci 25: 8048-8055, 2005.
18. Cohen AS, Raymond CR, and Abraham WC. Priming of long-term potentiation induced by activation of metabotropic glutamate receptors coupled to phospholipase C. Hippocampus 8: 160-70, 1998.
19. Cohen-Cory S. The developing synapse: construction and modulation of synaptic structures and circuits. Science 298: 770-776, 2002.
20. Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, Weiler IJ, and Greenough WT. Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci USA 94: 5401-5404, 1997.
21. Cudmore RH and Turrigiano GG. Long-term potentiation of intrinsic excitability in LV visual cortical neurons. J Neurophysiol 92: 341-348, 2004.
22. Dan Y and Poo M-M Spike timing-dependent plasticity of neural circuits. Neuron 44: 23-30, 2004.
23. Daoudal G and Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 10: 456-465, 2003.
24. Desai NS, Cudmore RH, Nelson SB, and Turrigiano GG. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci 5: 783-789, 2002.
25. Desai NS and Walcott EC. Synaptic bombardment modulates muscarinic effects in forelimb motor cortex. J Neurosci 26: 2215-2226, 2006.
26. Duguid I and Sjöström PJ. Novel presynaptic mechanisms for coincidence detection in synaptic plasticity. Curr Opin Neurobiol 16:1-11, 2006.
27. Eckert MJ and Racine RJ. Metabotropic glutamate receptors contribute to neocortical synaptic plasticity in vivo. Neuroreport 15: 2685-2689, 2004.
28. Ehrlich I and Malinow R. Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J Neurosci 24: 916-927, 2004.
29. Feldman DE. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27: 45-56, 2000.
30. Feldman DE and Brecht M. Map plasticity in somatosensory cortex. Science 310: 810-815, 2005.
31. Fox K and Wong ROL. A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48: 465-477, 2005.
32. Franceschetti S, Sancini G, Panzica F, Radici C, and Avanzini G. Postnatal differentiation of firing properties and morphological characteristics in layer V pyramidal neurons of the sensorimotor cortex. Neuroscience 83: 1013-1024, 1998.
33. Froemke RC and Dan Y. Spike timing-dependent synaptic modification induced by natural spike trains. Nature 416: 433-438, 2002.
34. Galvez R and Greenough WT. Sequence of abnormal dendritic spine development in primary somatosensory cortex of a mouse model of the Fragile X mental retardation syndrome. Am Med Genet 135A: 155-160, 2005.
35. Godfraind JM, Reyniers E, De Boulle K, D'Hooge R, De Deyn PP, Bakker CE, Oostra BA, Kooy RF, and Willems PJ. Long-term potentiation in the hippocampus of fragile X knockout mice. Am J Med Genet 64: 246-251, 1996.
36. Harney SC, Rowan M, and Anwyl R. Long-term depression of NMDA receptor-mediated synaptic transmission is dependent on activation of metabotropic glutamate receptors and is altered to long-term potentiation by low intracellular calcium buffering. J Neurosci 26: 1128-1132, 2006.
37. Hayashi Y and Majewska AK. Dendritic spine geometry: functional implication and regulation. Neuron 46: 529-532, 2005.
38. Holscher C. Metabotropic glutamate receptors control gating of spike transmission in the hippocampus area CA1. Pharmacol Biochem Behav 73:307-316, 2002.
39. Huber KM, Kayser MS, and Bear MF. Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288(5469): 1254-1257, 2000.
40. Huber KM, Gallagher SM, Warren ST, and Bear MF. Altered synaptic plasticity in a mouse model of Fragile X mental retardation. Proc Natl Acad Sci USA 99: 7746-7750, 2002.
41. Huemmeke M, Eysel UT, and Mittmann T. Metabotropic glutamate receptors mediate expression of LTP in slices of rat visual cortex. Eur J Neurosci 15: 1641-1645, 2002.
42. Ireland DR and Abraham WC. Group I mGluRs increase excitability of hippocampal CA1 pyramidal neurons by a PLC-independent mechanism. J Neurophysiol 88: 107-116, 2002.
43. Irwin SA, Galvez R, and Greenough WT. Dendritic spinestructural snomalies in fragile X mental retardation syndrome. Cereb Cortex 10: 1038-1044, 2000.
44. Katz LC and Crowley JC. Development of cortical circuits: lessons from ocular dominance columns. Nat Rev Neurosci 3: 34-42, 2002.
45. Koekkoek SK, Yamaguchi K, Milojkovic BA, Dortland BR, Ruigrok TJ, Maex R, De Graaf W, Smit AE, VanderWerf F, Bakker CE, Willemsen R, Ikeda T, Kakizawa S, Onodera K, Nelson DL, Mientjes E, Joosten M, De Schutter E, Oostra BA, Ito M, and De Zeeuw CI. Deletion of Fmr1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron 47: 339-352, 2005.
46. Larson J, Jessen RE, Kim D, Fine AS, and du Hoffmann J. Age-dependent and selective impairment of long-term potentiation in the anterior piriform cortex of mice lacking the Fragile X mental retardation protein. J Neurosci 25: 9460-9469, 2005.
47. Lendvai B, Stern E, Chen B, and Svoboda K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404: 876-881, 2000.
48. Li J, Pelletier MR, Perez Velazquez JL, and Carlen PL. Reduced cortical synaptic plasticity and GluR1 expression associated with Fragile X mental retardation protein deficiency. Mol Cell Neurosci 19: 138-151, 2002.
49. Lopez-Bendito G, Shigemoto R, Fairen A, and Lujan R. Differential distribution of group I metabotropic glutamate receptors during rat cortical development. Cereb Cortex 12: 625-638, 2002.
50. Malenka RC and Bear MF. LTP and LTD: an embarrassment of riches. Neuron 44: 5-21, 2004.
51. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, and Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4: 1086-1092, 2001.
52. Matsuzaki M, Honkura N, Ellis-Davies GC, and Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 429: 761-7666, 2004.
53. McBride SM, Choi CH, Wang Y, Liebelt D, Braunstein E, Ferreiro D, Sehgal A, Siwicki KK, Dockendorff TC, Nguyen HT, McDonald TV, and Jongens TA. Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of fragile X syndrome. Neuron 45: 753-764, 2005.
54. Micheva KD and Beaulieu C. Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry. J Comp Neurol 373: 340-354, 1996.
55. Miura M, Watanabe M, Offermanns S, Simon MI, and Kano M. Group I metabotropic glutamate receptor signaling via Galpha q/Galpha 11 secures the induction of long-term potentiation in the hippocampal area CA1. J Neurosci 22: 8379-8390, 2002.
56. Morris SH, Knevett S, Lerner EG, and Bindman LJ. Group I mGluR agonist DHPG facilitates the induction of LTP in rat prelimbic cortex in vitro. J Neurophysiol 82: 1927-1933, 1999.
57. Myme CIO, Sugino K, Turrigiano GG, and Nelson SB. The NMDA-to-AMPA ratio at synapses onto layer 2/3 pyramidal neurons is conserved across prefrontal and visual cortices. J Neurophysiol 90: 771-779, 2003.
58. Nimchinsky EA, Oberlander AM, and Svoboda K. Abnormal development of dendritic spines in Fmr1 knock-out mice. J Neurosci 21: 5139-5146, 2001.
59. Nosyreva ED and Huber KM. Metabotropic receptor-dependent long-term depression persists in the absence of protein synthesis in the mouse model of fragile X syndrome. J Neurophysiol 95: 3291-3295, 2006.
60. O'Donnell WT and Warren ST. A decade of molecular studies of fragile X syndrome. Annu Rev Neurosci 25: 315-338, 2002.
61. Paradee W, Melikian HE, Rasmussen DL, Kenneson A, Conn PJ, and Warren ST. Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience 94: 185-192, 1999.
62. Raymond CR, Thompson VL, Tate WP, and Abraham WC. Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong longterm potentiation. J Neurosci 20: 969-976, 2000.
63. Savić N, Lüthi A, Gähwiler BH, and McKinney RA. NMDA receptor blockade during development lowers long-term potentiation threshold without affecting dynamic range of CA3-CA1 synapses. Proc Natl Acad Sci USA 100: 5503-5508, 2003.
64. Sawtell NB, Huber KM, Roder JC, and Bear MF. Induction of NMDA receptor-dependent long-term depression in visual cortex does not require metabotropic glutamate receptors. J Neurophysiol 82: 3594-3597, 1999.
65. Segal M. Dendritic spines and long-term plasticity. Nat Rev Neurosci 6:277-284, 2005.
66. Sourdet V, Russier M, Daoudal G, Ankri N, and Debanne D. Long-term enhancement of neuronal excitability and temporal fidelity mediated by metabotropic glutamate receptor subtype 5. J Neurosci 23: 10238-10248, 2003.
67. Sjöström PJ, Turrigiano GG, and Nelson SB. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32: 1149-1164, 2001.
68. Sjöström PJ, Turrigiano GG, and Nelson SB. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39: 641-654, 2003.
69. Stein V, House DR, Bredt DS, and Nicoll RA. Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression.J Neurosci 23: 5503-5506, 2003.
70. Stern EA, Maravall M, and Svoboda K. Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron 31: 305-315, 2001.
71. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, and Otterson OP. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat Neurosci 2: 618-624, 1999.
72. Thompson KJ, Mata ML, Orfila JE, Barea-Rodriguez EJ, and Martinez JL Jr. Metabotropic glutamate receptor antagonist AIDA blocks induction of mossy fiber-CA3 LTP in vivo. J Neurophysiol 93: 2668-2673, 2005.
73. Todd PK, Mack KJ, and Malter JS. The fragile X mental retardation protein is required for type-I metabotropic glutamate receptor-dependent translation of PSD-95. Proc Natl Acad Sci USA 100: 14374-14378, 2003.
74. Tsay D and Yuste R. On the electrical function of dendritic spines. Trends Neurosci 27: 77-83, 2004.
75. Turner G, Webb T, Wake S, and Robinson H. Prevalence of Fragile X syndrome. Am J Med Genet 64: 196-197, 1996.
76. Turrigiano GG and Nelson SB. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5: 97-107, 2004.
77. Vanderklish PW and Edelman GM. Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc Natl Acad Sci USA 99: 1639-1644, 2002.
78. Vanderklish PW and Edelman GM. Differential translation and fragile X syndrome. Genes Brain Behav 4: 360-384, 2005.
79. Xu J, Kang N, Jiang L, Nedergaard M, and Kang J. Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J Neurosci 25: 1750-1760, 2005.
80. Yan QJ, Asfo-Adjei PK, Arnold HM, Brown RE, and Bauchwitz RP. A phenotypic and molecular characterization of the Fmr1-tm1Cgr Fragile X mouse. Genes Brain Behav 3: 337-359, 2004.
81. Yuste R and Bonhoeffer T. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5:24 -34, 2004.
82. Zhang W and Linden DJ. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4: 885-900, 2003.
83. Zhao MG, Toyoda H, Ko SW, Ding HK, Wu LJ, and Zhuo M. Deficits in trace fear memory and long-term potentiation in a mouse model for Fragile X syndrome. J Neurosci 25: 7385-7392, 2005.