Delayed in vitro development of Up states but normal network plasticity in Fragile X circuits

European Journal of Neuroscience

Volumn 42, Issue 6, 2015, Pages 2312-2321

  Motanis, Helen ^a   Buonomano, Dean ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Homeostatic plasticity; Mouse; Optogenetic stimulation; Organotypic slices; Spontaneous activity

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; FMR1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONNECTOME; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DOWN REGULATION; FEMALE; FRAGILE X SYNDROME; GENOTYPE; HOMEOSTASIS; IN VITRO STUDY; MALE; MOUSE; MUTANT; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; OPTOGENETICS; PRIORITY JOURNAL; WILD TYPE; ANIMAL; BRAIN CORTEX; DISEASE MODEL; ELECTROENCEPHALOGRAM; GENETICS; NERVE CELL; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN WAVES; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; IN VITRO TECHNIQUES; MALE; MICE; NERVE NET; NEURONAL PLASTICITY; NEURONS; OPTOGENETICS;

EID: 84942193852     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.13010     Document Type: Article

References (73)

1. Antar, L.N., Li, C., Zhang, H., Carroll, R.C. & Bassell, G.J. (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.
2. Bear, M.F., Huber, K.M. & Warren, S.T. (2004) The mGluR theory of fragile X mental retardation. Trends Neurosci., 27, 370-377.
3. Belmonte, M.K. & Bourgeron, T. (2006) Fragile X syndrome and autism at the intersection of genetic and neural networks. Nat. Neurosci., 9, 1221-1225.
4. Bolz, J. (1994) Cortical circuitry in a dish. Curr. Opin. Neurobiol., 4, 545-549.
5. Brager, D.H., Akhavan, A.R. & Johnston, D. (2012) Impaired dendritic expression and plasticity of h-channels in the fmr1(-/y) mouse model of fragile X syndrome. Cell Rep., 1, 225-233.
6. Brown, M.R., Kronengold, J., Gazula, V.R., Chen, Y., Strumbos, J.G., Sigworth, F.J., Navaratnam, D. & Kaczmarek, L.K. (2010) Fragile X mental retardation protein controls gating of the sodium-activated potassium channel Slack. Nat. Neurosci., 13, 819-821.
7. Brunning, J.L. & Kintz, B.L. (1970) Computational Handbook of Statistics, 3rd Edn. Scott, Foresman and Company, Glenview, IL.
8. Buonomano, D.V. (2003) Timing of neural responses in cortical organotypic slices. Proc. Natl. Acad. Sci. USA, 100, 4897-4902.
9. Buonomano, D.V. & Merzenich, M.M. (1998) Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci., 21, 149-186.
10. Bureau, I., Shepherd, G.M.G. & Svoboda, K. (2008) Circuit and plasticity defects in the developing somatosensory cortex of Fmr1 knock-out mice. J. Neurosci., 28, 5178-5188.
11. Chauvette, S., Volgushev, M. & Timofeev, I. (2010) Origin of active states in local neocortical networks during slow sleep oscillation. Cereb. Cortex, 20, 2660-2674.
12. Chen, X., Rochefort, N.L., Sakmann, B. & Konnerth, A. (2013) Reactivation of the same synapses during spontaneous up states and sensory stimuli. Cell Rep., 4, 31-39.
13. Colonnese, M.T., Kaminska, A., Minlebaev, M., Milh, M., Bloem, B., Lescure, S., Moriette, G., Chiron, C., Ben-Ari, Y. & Khazipov, R. (2010) A conserved switch in sensory processing prepares developing neocortex for vision. Neuron, 67, 480-498.
14. Crunelli, V. & Hughes, S.W. (2010) The slow (<1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat. Neurosci., 13, 9-17.
15. Cruz-Martin, A., Crespo, M. & Portera-Cailliau, C. (2010) Delayed stabilization of dendritic spines in fragile X mice. J. Neurosci., 30, 7793-7803.
16. Curia, G., Papouin, T., Seguela, P. & Avoli, M. (2009) Downregulation of tonic GABAergic inhibition in a mouse model of fragile X syndrome. Cereb. Cortex, 19, 1515-1520.
17. De Simoni, A., Griesinger, C.B. & Edwards, F.A. (2003) Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. J. Physiol., 550, 135-147.
18. Deng, P.Y., Sojka, D. & Klyachko, V.A. (2011) Abnormal presynaptic short-term plasticity and information processing in a mouse model of fragile X syndrome. J. Neurosci., 31, 10971-10982.
19. Deng, P.Y., Rotman, Z., Blundon, J.A., Cho, Y., Cui, J., Cavalli, V., Zakharenko, S.S. & Klyachko, V.A. (2013) FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron, 77, 696-711.
20. Desai, N.S., Casimiro, T.M., Gruber, S.M. & Vanderklish, P.W. (2006) Early postnatal plasticity in neocortex of Fmr1 knockout Mice. J. Neurophysiol., 96, 1734-1745.
21. Destexhe, A. (2011) Intracellular and computational evidence for a dominant role of internal network activity in cortical computations. Curr. Opin. Neurobiol., 21, 717-725.
22. Echevarria, D. & Albus, K. (2000) Activity-dependent development of spontaneous bioelectric activity in organotypic cultures of rat occipital cortex. Brain Res. Dev. Brain Res., 123, 151-164.
23. Frankland, P.W., Wang, Y., Rosner, B., Shimizu, T., Balleine, B.W., Dykens, E.M., Ornitz, E.M. & Silva, A.J. (2004) Sensorimotor gating abnormalities in young males with fragile X syndrome and Fmr1-knockout mice. Mol. Psychiatr., 9, 417-425.
24. Gibson, J.R., Bartley, A.F., Hays, S.A. & Huber, K.M. (2008) Imbalance of neocortical excitation and inhibition and altered UP states reflect network hyperexcitability in the mouse model of fragile X syndrome. J. Neurophysiol., 100, 2615-2626.
25. Goel, A. & Buonomano, D.V. (2013) Chronic electrical stimulation homeostatically decreases spontaneous activity, but paradoxically increases evoked network activity. J. Neurophysiol., 109, 1824-1836.
26. Goncalves, J.T., Anstey, J.E., Golshani, P. & Portera-Cailliau, C. (2013) Circuit level defects in the developing neocortex of Fragile X mice. Nat. Neurosci., 16, 903-909.
27. Goold, C.P. & Nicoll, R.A. (2010) Single-cell optogenetic excitation drives homeostatic synaptic depression. Neuron, 68, 512-528.
28. Greenough, W.T., Hwang, H.M. & Gorman, C. (1985) Evidence for active synapse formation or altered postsynaptic metabolism in visual cortex of rats reared in complex environments. Proc. Natl. Acad. Sci. USA, 82, 4549-4552.
29. Gross, C., Yao, X., Pong, D.L., Jeromin, A. & Bassell, G.J. (2011) Fragile X mental retardation protein regulates protein expression and mRNA translation of the potassium channel Kv4.2. J. Neurosci., 31, 5693-5698.
30. Hagerman, P.J. & Stafstrom, C.E. (2009) Origins of epilepsy in fragile X syndrome. Epilepsy Curr., 9, 108-112.
31. Haider, B., Duque, A., Hasenstaub, A.R. & McCormick, D.A. (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J. Neurosci., 26, 4535-4545.
32. Hanson, J.E. & Madison, D.V. (2007) Presynaptic FMR1 genotype influences the degree of synaptic connectivity in a mosaic mouse model of fragile X syndrome. J. Neurosci., 27, 4014-4018.
33. Harlow, E.G., Till, S.M., Russell, T.A., Wijetunge, L.S., Kind, P. & Contractor, A. (2010) Critical period plasticity is disrupted in the barrel cortex of FMR1 knockout mice. Neuron, 65, 385-398.
34. Hays, S.A., Huber, K.M. & Gibson, J.R. (2011) Altered neocortical rhythmic activity states in Fmr1 KO mice are due to enhanced mGluR5 signaling and involve changes in excitatory circuitry. J. Neurosci., 31, 14223-14234.
35. He, C.X. & Portera-Cailliau, C. (2013) The trouble with spines in fragile X syndrome: density, maturity and plasticity. Neuroscience, 251, 120-128.
36. He, Q., Nomura, T., Xu, J. & Contractor, A. (2014) The developmental switch in GABA polarity is delayed in Fragile X mice. J. Neurosci., 34, 446-450.
37. Holtmaat, A. & Svoboda, K. (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci., 10, 647-658.
38. Hubel, D.H. & Wiesel, T.N. (1963) Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J. Neurophysiol., 26, 994-1002.
39. Huber, K.M., Gallagher, S.M., Warren, S.T. & Bear, M.F. (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. USA, 99, 7746-7750.
40. Irwin, S.A., Galvez, R. & Greenough, W.T. (2000) Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cereb. Cortex, 10, 1038-1044.
41. Johnson, H.A. & Buonomano, D.V. (2007) Development and plasticity of spontaneous activity and Up states in cortical organotypic slices. J. Neurosci., 27, 5915-5925.
42. Kim, H., Gibboni, R., Kirkhart, C. & Bao, S. (2013) Impaired critical period plasticity in primary auditory cortex of Fragile X model mice. J. Neurosci., 33, 15686-15692.
43. Kirkwood, A., Lee, H.-K. & Bear, M.F. (1995) Co-regulation of long-term potentiation and experience-dependent synaptic plasticity in visual cortex by age and experience. Nature, 375, 328-331.
44. Larson, J., Jessen, R.E., Kim, D., Fine, A.K. & du Hoffmann, J. (2005) 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.
45. Lee, H.Y. & Jan, L.Y. (2012) Fragile X syndrome: mechanistic insights and therapeutic avenues regarding the role of potassium channels. Curr. Opin. Neurobiol., 22, 887-894.
46. MacLean, J.N., Watson, B.O., Aaron, G.B. & Yuste, R. (2005) Internal dynamics determine the cortical response to thalamic stimulation. Neuron, 48, 811-823.
47. Mann, E.O., Kohl, M.M. & Paulsen, O. (2009) Distinct roles of GABA(A) and GABA(B) receptors in balancing and terminating persistent cortical activity. J. Neurosci., 29, 7513-7518.
48. Meredith, R.M., Holmgren, C.D., Weidum, M., Burnashev, N. & Mansvelder, H.D. (2007) Increased threshold for spike-timing-dependent plasticity is caused by unreliable calcium signaling in mice lacking Fragile X gene Fmr1. Neuron, 54, 627-638.
49. Miller, L.J., McIntosh, D.N., McGrath, J., Shyu, V., Lampe, M., Taylor, A.K., Tassone, F., Neitzel, K., Stackhouse, T. & Hagerman, R.J. (1999) Electrodermal responses to sensory stimuli in individuals with fragile X syndrome: a preliminary report. Am. J. Med. Genet., 83, 268-279.
50. Musumeci, S.A., Hagerman, R.J., Ferri, R., Bosco, P., Dalla Bernardina, B., Tassinari, C.A., De Sarro, G.B. & Elia, M. (1999) Epilepsy and EEG findings in males with fragile X syndrome. Epilepsia, 40, 1092-1099.
51. Nimchinsky, E.A., Oberlander, A.M. & Svoboda, K. (2001) Abnormal development of dendritic spines in FMR1 knock-out mice. J. Neurosci., 21, 5139-5146.
52. O'Donnell, W.T. & Warren, S.T. (2002) A decade of molecular studies of fragile X syndrome. Annu. Rev. Neurosci., 25, 315-338.
53. Olmos-Serrano, J.L., Paluszkiewicz, S.M., Martin, B.S., Kaufmann, W.E., Corbin, J.G. & Huntsman, M.M. (2010) Defective GABAergic neurotransmission and pharmacological rescue of neuronal hyperexcitability in the amygdala in a mouse model of fragile X syndrome. J. Neurosci., 30, 9929-9938.
54. Padmashri, R., Reiner, B.C., Suresh, A., Spartz, E. & Dunaevsky, A. (2013) Altered structural and functional synaptic plasticity with motor skill learning in a mouse model of fragile X syndrome. J. Neurosci., 33, 19715-19723.
55. Paluszkiewicz, S.M., Martin, B.S. & Huntsman, M.M. (2011a) Fragile X syndrome: the GABAergic system and circuit dysfunction. Dev. Neurosci., 33, 349-364.
56. Paluszkiewicz, S.M., Olmos-Serrano, J.L., Corbin, J.G. & Huntsman, M.M. (2011b) Impaired inhibitory control of cortical synchronization in fragile X syndrome. J. Neurophysiol., 106, 2264-2272.
57. Portera-Cailliau, C. (2012) Which comes first in fragile x syndrome, dendritic spine dysgenesis or defects in circuit plasticity? Neuroscientist, 18, 28-44.
58. Poskanzer, K.E. & Yuste, R. (2011) Astrocytic regulation of cortical UP states. Proc. Natl. Acad. Sci. USA, 108, 18453-18458.
59. Ramakers, G.J., Corner, M.A. & Habets, A.M. (1990) Development in the absence of spontaneous bioelectric activity results in increased stereotyped burst firing in cultures of dissociated cerebral cortex. Exp. Brain Res., 79, 157-166.
60. Rioult-Pedotti, M.S., Friedman, D. & Donoghue, J.P. (2000) Learning-induced LTP in neocortex. Science, 290, 533-536.
61. Routh, B.N., Johnston, D. & Brager, D.H. (2013) Loss of functional A-type potassium channels in the dendrites of CA1 pyramidal neurons from a mouse model of fragile X syndrome. J. Neurosci., 33, 19442-19450.
62. Runfeldt, M.J., Sadovsky, A.J. & MacLean, J.N. (2014) Acetylcholine functionally reorganizes neocortical microcircuits. J. Neurophysiol., 112, 1205-1216.
63. Santoro, M.R., Bray, S.M. & Warren, S.T. (2012) Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Ann. Rev. Pathol., 7, 219-245.
64. Soden, M.E. & Chen, L. (2010) Fragile X protein FMRP is required for homeostatic plasticity and regulation of synaptic strength by retinoic acid. J. Neurosci., 30, 16910-16921.
65. Stoppini, L., Buchs, P.A. & Muller, D. (1991) A simple method for organotypic cultures of nervous tissue. J. Neurosci. Meth., 37, 173-182.
66. Testa-Silva, G., Loebel, A., Giugliano, M., de Kock, C.P., Mansvelder, H.D. & Meredith, R.M. (2012) Hyperconnectivity and slow synapses during early development of medial prefrontal cortex in a mouse model for mental retardation and autism. Cereb. Cortex, 22, 1333-1342.
67. Thompson, I. (1997) Cortical development: a role for spontaneous activity? Curr. Biol., 7, R324-R326.
68. Trachtenberg, J.T., Chen, B.E., Knott, G.W., Feng, G., Sanes, J.R., Welker, E. & Svoboda, K. (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature, 420, 788-794.
69. Van der Molen, M.J., Van der Molen, M.W., Ridderinkhof, K.R., Hamel, B.C., Curfs, L.M. & Ramakers, G.J. (2012) Auditory and visual cortical activity during selective attention in fragile X syndrome: a cascade of processing deficiencies. Clin. Neurophysiol., 123, 720-729.
70. Verkerk, A.J., Pieretti, M., Sutcliffe, J.S., Fu, Y.H., Kuhl, D.P., Pizzuti, A., Reiner, O., Richards, S., Victoria, M.F., Zhang, F.P., Eussen, B.E., van Ommen, G.-J.B., Blonden, L.A.J., Riggins, G.J., Chastain, J.L., Kunst, C.B., Galjaard, H., Caskey, C.T., Nelson, D.L., Oostra, B.A. & Warren, S.T. (1991) Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell, 65, 905-914.
71. Vislay, R.L., Martin, B.S., Olmos-Serrano, J.L., Kratovac, S., Nelson, D.L., Corbin, J.G. & Huntsman, M.M. (2013) Homeostatic Responses fail to correct defective amygdala inhibitory circuit maturation in Fragile X syndrome. J. Neurosci., 33, 7548-7558.
72. Wang, L., Fontanini, A. & Maffei, A. (2012) Experience-dependent switch in sign and mechanisms for plasticity in layer 4 of primary visual cortex. J. Neurosci., 32, 10562-10573.
73. Zhang, Y., Bonnan, A., Bony, G., Ferezou, I., Pietropaolo, S., Ginger, M., Sans, N., Rossier, J., Oostra, B., LeMasson, G. & Frick, A. (2014) Dendritic channelopathies contribute to neocortical and sensory hyperexcitability in Fmr1(-/y) mice. Nat. Neurosci., 17, 1701-1709.