GABAergic dysfunction in pediatric neuro-developmental disorders

Frontiers in Cellular Neuroscience

Volumn 7, Issue DEC, 2013, Pages

  Smith Hicks, Constance L ^a,b  

^a KENNEDY KRIEGER INSTITUTE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Circuits; Critical period; Disease; PV interneurons; Synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA3; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA4; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA5; 4 AMINOBUTYRIC ACID A RECEPTOR BETA2; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA3; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; ARBACLOFEN; BENZYL [3 [[1 (3, 4 DICHLOROPHENYL) ETHYL] AMINO] 2 HYDROXYPROPYL] PHOSPHINIC ACID; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; GABOXADOL; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; METHYL CPG BINDING PROTEIN 2; NOOTROPIC AGENT; PARVALBUMIN; PENTETRAZOLE; RO 4938581; UNCLASSIFIED DRUG;

AUTISM; CLINICAL TRIAL (TOPIC); DEVELOPMENTAL DISORDER; DOWN SYNDROME; FRAGILE X SYNDROME; GABAERGIC SYSTEM; HIPPOCAMPAL CA1 REGION; HUMAN; LEARNING; MEMORY; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NEUROLOGIC DISEASE; NONHUMAN; PROTEIN EXPRESSION; RETT SYNDROME; REVIEW; STRATUM LACUNOSUM MOLECULARE; SYNAPTIC TRANSMISSION; THALAMUS RETICULAR NUCLEUS;

EID: 84891098197     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00269     Document Type: Review

References (100)

1. Adusei, D. C., Pacey, L. K., Chen, D., and Hampson, D. R. (2010). Early developmental alterations in GABAergic protein expression in fragile X knockout mice. Neuropharmacology 59, 167-171. doi: 10.1016/j.neuropharm.2010.05.002
2. Asaka, Y., Jugloff, D. G., Zhang, L., Eubanks, J. H., and Fitzsimonds, R. M. (2006). Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol. Dis. 21, 217-227. doi: 10.1016/j.nbd.2005.07.005
3. Atallah, B. V., Bruns, W., Carandini, M., and Scanziani, M. (2012). Parvalbuminexpressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73, 159-170. doi: 10.1016/j.neuron.2011.12.013
4. Bavelier, D., Levi, D. M., Li, R. W., Dan, Y., and Hensch, T. K. (2010). Removing brakes on adult brain plasticity: from molecular to behavioral interventions. J. Neurosci. 30, 14964-14971. doi: 10.1523/JNEUROSCI.4812-10.2010
5. Begenisic, T., Spolidoro, M., Braschi, C., Baroncelli, L., Milanese, M., Pietra, G., et al. (2011). Environmental enrichment decreases GABAergic inhibition and improves cognitive abilities, synaptic plasticity, and visual functions in a mouse model of Down syndrome. Front. Cell. Neurosci. 5:29. doi:10.3389/fncel.2011.00029
6. Belichenko, N. P., Belichenko, P. V., Kleschevnikov, A. M., Salehi, A., Reeves, R. H., and Mobley, W. C. (2009). The "Down syndrome critical region" is sufficient in the mouse model to confer behavioral, neurophysiological, and synaptic phenotypes characteristic of Down syndrome. J. Neurosci. 29, 5938-5948. doi: 10.1523/JNEUROSCI.1547-09.2009
7. Belichenko, P. V., Masliah, E., Kleschevnikov, A. M., Villar, A. J., Epstein, C. J., Salehi, A., et al. (2004). Synaptic structural abnormalities in the Ts65Dn mouse model of Down Syndrome. J. Comp. Neurol. 480, 281-298. doi: 10.1002/cne. 20337
8. Ben-Ari, Y. (2002). Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739. doi: 10.1038/nrn920
9. Berry-Kravis, E. M., Hessl, D., Rathmell, B., Zarevics, P., Cherubini, M., Walton-Bowen, K., et al. (2012). Effects of STX209 (arbaclofen) on neurobehavioral function in children and adults with fragile X syndrome: a randomized, controlled, phase 2 trial. Sci. Transl. Med. 4, 152ra127. doi: 10.1126/scitranslmed. 3004214
10. Best, T. K., Cramer, N. P., Chakrabarti, L., Haydar, T. F., and Galdzicki, Z. (2012). Dysfunctional hippocampal inhibition in the Ts65Dn mouse model of Down syndrome. Exp. Neurol. 233, 749-757. doi: 10.1016/j.expneurol.2011.11.033
11. Best, T. K., Siarey, R. J., and Galdzicki, Z. (2007). Ts65Dn, a mouse model of Down syndrome, exhibits increased GABAB-induced potassium current. J. Neurophysiol. 97, 892-900. doi: 10.1152/jn.00626.2006
12. Blatt, G. J., Fitzgerald, C. M., Guptill, J. T., Booker, A. B., Kemper, T. L., and Bauman, M. L. (2001). Density and distribution of hippocampal neurotransmitter receptors in autism: an autoradiographic study. J. Autism Dev. Disord. 31, 537-543. doi: 10.1023/A:1013238809666
13. Braudeau, J., Delatour, B., Duchon, A., Pereira, P. L., Dauphinot, L., de Chaumont, F., et al. (2011). Specific targeting of the GABA-A receptor alpha5 subtype by a selective inverse agonist restores cognitive deficits in Down syndrome mice. J. Psychopharmacol. 25, 1030-1042. doi: 10.1177/0269881111405366
14. Brennan, F. X., Albeck, D. S., and Paylor, R. (2006). Fmr1 knockout mice are impaired in a leverpress escape/avoidance task. Genes Brain Behav. 5, 467-471. doi: 10.1111/j.1601-183X.2005.00183.x
15. Brun, V. H., Otnass, M. K., Molden, S., Steffenach, H. A., Witter, M. P., Moser, M. B., et al. (2002). Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296, 2243-2246. doi: 10.1126/science.1071089
16. Buxbaum, J. D., Silverman, J. M., Smith, C. J., Greenberg, D. A., Kilifarski, M., Reichert, J., et al. (2002). Association between a GABRB3 polymorphism and autism. Mol. Psychiatry 7, 311-316. doi: 10.1038/sj.mp.4001011
17. Cancedda, L., Fiumelli, H., Chen, K., and Poo, M. M. (2007). Excitatory GABA action is essential for morphological maturation of cortical neurons in vivo. J. Neurosci. 27, 5224-5235. doi: 10.1523/JNEUROSCI.5169-06.2007
18. Centonze, D., Rossi, S., Mercaldo, V., Napoli, I., Ciotti, M. T., De Chiara, V., et al. (2008). Abnormal striatal GABA transmission in the mouse model for the fragile X syndrome. Biol. Psychiatry 63, 963-973. doi: 10.1016/j.biopsych.2007.09.008
19. Chakrabarti, L., Best, T. K., Cramer, N. P., Carney, R. S., Isaac, J. T., Galdzicki, Z., et al. (2010). Olig1 and Olig2 triplication causes developmental brain defects in Down syndrome. Nat. Neurosci. 13, 927-934. doi: 10.1038/nn.2600
20. Chang, Q., Khare, G., Dani, V., Nelson, S., and Jaenisch, R. (2006). The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression. Neuron 49, 341-348. doi: 10.1016/j.neuron.2005.12.027
21. Cook, E. H. Jr., Courchesne, R. Y., Cox, N. J., Lord, C., Gonen, D., Guter, S. J., et al. (1998). Linkage-disequilibrium mapping of autistic disorder, with 15q11-13 markers. Am. J. Hum. Genet. 62, 1077-1083. doi: 10.1086/301832
22. Costa, A. C., and Grybko, M. J. (2005). Deficits in hippocampal CA1 LTP induced by TBS but not HFS in the Ts65Dn mouse: a model of Down syndrome. Neurosci. Lett. 382, 317-322. doi: 10.1016/j.neulet.2005.03.031
23. Dani, V. S., Chang, Q., Maffei, A., Turrigiano, G. G., Jaenisch, R., and Nelson, S. B. (2005). Reduced cortical activity due to a shift in the balance between excitation and inhibition in a mouse model of Rett syndrome. Proc. Natl. Acad. Sci. U.S.A. 102, 12560-12565. doi: 10.1073/pnas.0506071102
24. D'Hulst, C., Atack, J. R., and Kooy, R. F. (2009). The complexity of the GABAA receptor shapes unique pharmacological profiles. Drug Discov. Today 14,866-875. doi: 10.1016/j.drudis.2009.06.009
25. D'Hulst, C., and Kooy, R. F. (2009). Fragile X syndrome: from molecular genetics to therapy. J. Med. Genet. 46, 577-584. doi: 10.1136/jmg.2008.064667
26. Durand, S., Patrizi, A., Quast, K. B., Hachigian, L., Pavlyuk, R., Saxena, A., et al. (2012). NMDA receptor regulation prevents regression of visual cortical function in the absence of Mecp2. Neuron 76, 1078-1090. doi: 10.1016/j.neuron.2012.12.004
27. El Idrissi, A., Ding, X. H., Scalia, J., Trenkner, E., Brown, W. T., and Dobkin, C. (2005). Decreased GABA(A) receptor expression in the seizure-prone fragile X mouse. Neurosci. Lett. 377, 141-146. doi: 10.1016/j.neulet.2004.11.087
28. Fernandez, F., and Garner, C. C. (2008). Episodic-like memory in Ts65Dn, a mouse model of Down syndrome. Behav. Brain Res. 188, 233-237. doi: 10.1016/j.bbr.2007.09.015
29. Fernandez, F., Morishita, W., Zuniga, E., Nguyen, J., Blank, M., Malenka, R. C., et al. (2007). Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome. Nat. Neurosci. 10, 411-413. doi: 10.1038/nn1860
30. Gantois, I., Vandesompele, J., Speleman, F., Reyniers, E., D'Hooge, R., Severijnen, L. A., et al. (2006). Expression profiling suggests underexpression of the GABA(A) receptor subunit delta in the fragile X knockout mouse model. Neurobiol. Dis. 21, 346-357. doi: 10.1016/j.nbd.2005.07.017
31. Gibson, J. R., Bartley, A. F., Hays, S. A., and 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. doi: 10.1152/jn.90752.2008
32. Hagerman, R. J., Ono, M. Y., and Hagerman, P. J. (2005). Recent advances in fragile X: a model for autism and neurodegeneration. Curr. Opin. Psychiatry 18, 490-496. doi: 10.1097/01.yco.0000179485.39520.b0
33. Harada, M., Taki, M. M., Nose, A., Kubo, H., Mori, K., Nishitani, H., et al. (2011). Non-invasive evaluation of the GABAergic/glutamatergic system in autistic patients observed by MEGA-editing proton MR spectroscopy using a clinical 3 tesla instrument. J. Autism Dev. Disord. 41, 447-454. doi: 10.1007/s10803-0101065-0
34. Harashima, C., Jacobowitz, D. M., Witta, J., Borke, R. C., Best, T. K., Siarey, R. J., et al. (2006). Abnormal expression of the G-protein-activated inwardly rectifying potassium channel 2 (GIRK2) in hippocampus, frontal cortex, and substantia nigra of Ts65Dn mouse: a model of Down syndrome. J. Comp. Neurol. 494, 815-833. doi: 10.1002/cne.20844
35. Heimel, J. A., van Versendaal, D., and Levelt, C. N. (2011). The role of GABAergic inhibition in ocular dominance plasticity. Neural Plast. 2011, 391763. doi: 10.1155/2011/391763
36. Henderson, C., Wijetunge, L., Kinoshita, M. N., Shumway, M., Hammond, R. S., Postma, F. R., et al. (2012). Reversal of disease-related pathologies in the fragile X mouse model by selective activation of GABAB receptors with arbaclofen. Sci. Transl. Med. 4, 152ra128. doi: 10.1126/scitranslmed.3004218
37. Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888. doi: 10.1038/nrn1787
38. Hevers, W., and Luddens, H. (1998). The diversity of GABAA receptors. Pharmacological and electrophysiological properties of GABAA channel subtypes. Mol. Neurobiol. 18, 35-86. doi: 10.1007/BF02741459
39. Hong, E. J., McCord, A. E., and Greenberg, M. E. (2008). A biological function for the neuronal activity-dependent component of Bdnf transcription in the development of cortical inhibition. Neuron 60, 610-624. doi: 10.1016/j.neuron. 2008.09.024
40. Huang, Z. J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M. F., et al. (1999). BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98, 739-755. doi: 10.1016/S0092-8674(00)81509-3
41. Kapfer, C., Glickfeld, L. L., Atallah, B. V., and Scanziani, M. (2007). Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat. Neurosci. 10, 743-753. doi: 10.1038/nn1909
42. Katagiri, H., Fagiolini, M., and Hensch, T. K. (2007). Optimization of somatic inhibition at critical period onset in mouse visual cortex. Neuron 53, 805-812. doi: 10.1016/j.neuron.2007.02.026
43. Kaufmann, W. E., Cortell, R., Kau, A. S., Bukelis, I., Tierney, E., Gray, R. M., et al. (2004). Autism spectrum disorder in fragile X syndrome: communication, social interaction, and specific behaviors. Am. J. Med. Genet. A 129A, 225-234. doi: 10.1002/ajmg.a.30229
44. Kleschevnikov, A. M., Belichenko, P. V., Gall, J., George, L., Nosheny, R., Maloney, M. T., et al. (2012). Increased efficiency of the GABAA and GABAB receptormediated neurotransmission in the Ts65Dn mouse model of Down syndrome. Neurobiol. Dis. 45, 683-691. doi: 10.1016/j.nbd.2011.10.009
45. Kleschevnikov, A. M., Belichenko, P. V., Villar, A. J., Epstein, C. J., Malenka, R. C., and Mobley, W. C. (2004). Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J. Neurosci. 24, 8153-8160. doi: 10.1523/JNEUROSCI.1766-04.2004
46. Knudsen, E. I. (2004). Sensitive periods in the development of the brain and behavior. J. Cogn. Neurosci. 16, 1412-1425. doi: 10.1162/0898929042304796
47. Kohara, K., Yasuda, H., Huang, Y., Adachi, N., Sohya, K., and Tsumoto, T. (2007). A local reduction in cortical GABAergic synapses after a loss of endogenous brainderived neurotrophic factor, as revealed by single-cell gene knock-out method. J. Neurosci. 27, 7234-7244. doi: 10.1523/JNEUROSCI.1943-07.2007
48. Kullmann, D. M. (2011). Interneuron networks in the hippocampus. Curr. Opin. Neurobiol. 21, 709-716. doi: 10.1016/j.conb.2011.05.006
49. Liu, X., Novosedlik, N., Wang, A., Hudson, M. L., Cohen, I. L., Chudley, A. E., et al. (2009). The DLX1and DLX2 genes and susceptibility to autism spectrum disorders. Eur. J. Hum. Genet. 17, 228-235. doi: 10.1038/ejhg.2008.148
50. Lonetti, G., Angelucci, A., Morando, L., Boggio, E. M., Giustetto, M., and Pizzorusso, T. (2010). Early environmental enrichment moderates the behavioral and synaptic phenotype of MeCP2 null mice. Biol. Psychiatry 67, 657-665. doi: 10.1016/j.biopsych.2009.12.022
51. Lopez-Bendito, G., Shigemoto, R., Kulik, A., Vida, I., Fairen, A., and Lujan, R. (2004). Distribution of metabotropic GABA receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus during prenatal and postnatal development. Hippocampus 14, 836-848. doi: 10.1002/hipo.10221
52. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807. doi: 10.1038/nrn1519
53. Martinez-Cue, C., Martinez, P., Rueda, N., Vidal, R., Garcia, S., Vidal, V., et al. (2013). Reducing GABAA alpha5 receptor-mediated inhibition rescues functional and neuromorphological deficits in a mouse model of down syndrome. J. Neurosci. 33, 3953-3966. doi: 10.1523/JNEUROSCI.1203-12.2013
54. Marty, S., Wehrle, R., and Sotelo, C. (2000). Neuronal activity and brain-derived neurotrophic factor regulate the density of inhibitory synapses in organotypic slice cultures of postnatal hippocampus. J. Neurosci. 20, 8087-8095.
55. Maya Vetencourt, J. F., Sale, A., Viegi, A., Baroncelli, L., De Pasquale, R., O'Leary, O. F., et al. (2008). The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 320, 385-388. doi: 10.1126/science.1150516
56. McCauley, J. L., Olson, L. M., Delahanty, R., Amin, T., Nurmi, E. L., Organ, E. L., et al. (2004). A linkage disequilibrium map of the 1-Mb 15q12 GABA(A) receptor subunit cluster and association to autism. Am. J. Med. Genet. B Neuropsychiatr. Genet. 131B, 51-59. doi: 10.1002/ajmg.b.30038
57. Medrihan, L., Tantalaki, E., Aramuni, G., Sargsyan, V., Dudanova, I., Missler, M., et al. (2008). Early defects of GABAergic synapses in the brain stem of a MeCP2 mouse model of Rett syndrome. J. Neurophysiol. 99, 112-121. doi: 10.1152/jn.00826.2007
58. Meguro-Horike, M., Yasui, D. H., Powell, W., Schroeder, D. I., Oshimura, M., Lasalle, J. M., et al. (2011). Neuron-specific impairment of inter-chromosomal pairing and transcription in a novel model of human 15q-duplication syndrome. Hum. Mol. Genet. 20, 3798-3810. doi: 10.1093/hmg/ddr298
59. Mendez, M. A., Horder, J., Myers, J., Coghlan, S., Stokes, P., Erritzoe, D., et al. (2013). The brain GABA-benzodiazepine receptor alpha-5 subtype in autism spectrum disorder: a pilot [(11)C]Ro15-4513 positron emission tomography study. Neuropharmacology 68, 195-201. doi: 10.1016/j.neuropharm.2012.04.008
60. Menold, M. M., Shao, Y., Wolpert, C. M., Donnelly, S. L., Raiford, K. L., Martin, E. R., et al. (2001). Association analysis of chromosome 15 gabaa receptor subunit genes in autistic disorder. J. Neurogenet. 15, 245-259. doi: 10.3109/0167706010 9167380
61. Mitra, A., Blank, M., and Madison, D. V. (2012). Developmentally altered inhibition in Ts65Dn, a mouse model of Down syndrome. Brain Res. 1440, 1-8. doi: 10.1016/j.brainres.2011.12.034
62. Mohler, H. (2007). Molecular regulation of cognitive functions and developmental plasticity: impact of GABAA receptors. J. Neurochem. 102, 1-12. doi: 10.1111/j.1471-4159.2007.04454.x
63. Moretti, P., Levenson, J. M., Battaglia, F., Atkinson, R., Teague, R., Antalffy, B., et al. (2006). Learning and memory and synaptic plasticity are impaired in a mouse model of Rett syndrome. J. Neurosci. 26, 319-327. doi: 10.1523/JNEUROSCI. 2623-05.2006
64. Mori, T., Mori, K., Fujii, E., Toda, Y., Miyazaki, M., Harada, M., et al. (2012). Evaluation of the GABAergic nervous system in autistic brain: (123)I-iomazenil SPECT study. Brain Dev. 34, 648-654. doi: 10.1016/j.braindev.2011.10.007
65. Musumeci, S. A., Bosco, P., Calabrese, G., Bakker, C., De Sarro, G. B., Elia, M., et al. (2000). Audiogenic seizures susceptibility in transgenic mice with fragile X syndrome. Epilepsia 41, 19-23. doi: 10.1111/j.1528-1157.2000.tb01499.x
66. Nielsen, D. M., Derber, W. J., McClellan, D. A., and Crnic, L. S. (2002). Alterations in the auditory startle response in Fmr1 targeted mutant mouse models of fragile X syndrome. Brain Res. 927, 8-17. doi: 10.1016/S0006-8993(01)03309-1
67. Oblak, A., Gibbs, T. T., and Blatt, G. J. (2009). Decreased GABAA receptors and benzodiazepine binding sites in the anterior cingulate cortex in autism. Autism Res. 2, 205-219. doi: 10.1002/aur.88
68. Oblak, A. L., Gibbs, T. T., and Blatt, G. J. (2010). Decreased GABA(B) receptors in the cingulate cortex and fusiform gyrus in autism. J. Neurochem. 114, 1414-1423. doi: 10.1111/j.1471-4159.2010.06858.x
69. O'Donnell, W. T., and Warren, S. T. (2002). A decade of molecular studies of fragile X syndrome. Annu. Rev. Neurosci. 25, 315-338. doi: 10.1146/annurev.neuro. 25.112701.142909
70. Olmos-Serrano, J. L., Corbin, J. G., and Burns, M. P. (2011). The GABA(A) receptor agonist THIP ameliorates specific behavioral deficits in the mouse model of fragile X syndrome. Dev. Neurosci. 33, 395-403. doi: 10.1159/000332884
71. Olmos-Serrano, J. L., Paluszkiewicz, S. M., Martin, B. S., Kaufmann, W. E., Corbin, J. G., and 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. doi: 10.1523/JNEUROSCI.1714-10.2010
72. Olsen, R. W., and Sieghart, W. (2009). GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 56, 141-148. doi: 10.1016/j.neuropharm.2008.07.045
73. Pacey, L. K., Heximer, S. P., and Hampson, D. R. (2009). Increased GABA(B) receptor-mediated signaling reduces the susceptibility of fragile X knockout mice to audiogenic seizures. Mol. Pharmacol. 76, 18-24. doi: 10.1124/mol.109. 056127
74. Paluszkiewicz, S. M., Olmos-Serrano, J. L., Corbin, J. G., and Huntsman, M. M. (2011). Impaired inhibitory control of cortical synchronization in fragile X syndrome. J. Neurophysiol. 106, 2264-2272. doi: 10.1152/jn.00421.2011
75. Perez-Cremades, D., Hernandez, S., Blasco-Ibanez, J. M., Crespo, C., Nacher, J., and Varea, E. (2010). Alteration of inhibitory circuits in the somatosensory cortex of Ts65Dn mice, a model for Down's syndrome. J. Neural Transm. 117, 445-455. doi: 10.1007/s00702-010-0376-9
76. Pham, T. M., Nurse, S., and Lacaille, J. C. (1998). Distinct GABAB actions via synaptic and extrasynaptic receptors in rat hippocampus in vitro. J. Neurophysiol. 80, 297-308.
77. Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., and Maffei, L. (2002). Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251. doi: 10.1126/science.1072699
78. Rudolph, U., and Mohler, H. (2006). GABA-based therapeutic approaches: GABAA receptor subtype functions. Curr. Opin. Pharmacol. 6, 18-23. doi: 10.1016/j.coph.2005.10.003
79. Rueda, N., Florez, J., and Martinez-Cue, C. (2008). Chronic pentylenetetrazole but not donepezil treatment rescues spatial cognition in Ts65Dn mice, a model for Down syndrome. Neurosci. Lett. 433, 22-27. doi: 10.1016/j.neulet.2007.12.039
80. Sale, A., Maya Vetencourt, J. F., Medini, P., Cenni, M. C., Baroncelli, L., De Pasquale, R., et al. (2007). Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat. Neurosci. 10, 679-681. doi: 10.1038/nn1899
81. Sebat, J., Lakshmi, B., Malhotra, D., Troge, J., Lese-Martin, C., Walsh, T., et al. (2007). Strong association of de novo copy number mutations with autism. Science 316, 445-449. doi: 10.1126/science.1138659
82. Shao, Y., Cuccaro, M. L., Hauser, E. R., Raiford, K. L., Menold, M. M., Wolpert, C. M., et al. (2003). Fine mapping of autistic disorder to chromosome 15q11-q13 by use of phenotypic subtypes. Am. J. Hum. Genet. 72, 539-548. doi: 10.1086/ 367846
83. Siarey, R. J., Stoll, J., Rapoport, S. I., and Galdzicki, Z. (1997). Altered long-term potentiation in the young and old Ts65Dn mouse, a model for Down Syndrome. Neuropharmacology 36, 1549-1554. doi: 10.1016/S0028-3908(97)00157-3
84. Sieghart, W., and Sperk, G. (2002). Subunit composition, distribution and function of GABA(A) receptor subtypes. Curr. Top. Med. Chem. 2, 795-816. doi: 10.2174/1568026023393507
85. Silberberg, G., and Markram, H. (2007). Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53, 735-746. doi: 10.1016/j.neuron.2007.02.012
86. Sloviter, R. S., Ali-Akbarian, L., Elliott, R. C., Bowery, B. J., and Bowery, N. G. (1999). Localization of GABA(B) (R1) receptors in the rat hippocampus by immunocytochemistry and high resolution autoradiography, with specific reference to its localization in identified hippocampal interneuron subpopulations. Neuropharmacology 38, 1707-1721. doi: 10.1016/S0028-3908(99)00132-X
87. Sodickson, D. L., and Bean, B. P. (1996). GABAB receptor-activated inwardly rectifying potassium current in dissociated hippocampal CA3 neurons. J. Neurosci. 16, 6374-6385.
88. Soleman, S., Filippov, M. A., Dityatev, A., and Fawcett, J. W. (2013). Targeting the neural extracellular matrix in neurological disorders. Neuroscience 253, 194-213. doi: 10.1016/j.neuroscience.2013.08.050
89. Somogyi, P., and Klausberger, T. (2005). Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. 562, 9-26. doi: 10.1113/jphysiol.2004.078915
90. Somogyi, P., Tamas, G., Lujan, R., and Buhl, E. H. (1998). Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26, 113-135. doi: 10.1016/S0165-0173(97)00061-1
91. Southwell, D. G., Froemke, R. C., Alvarez-Buylla, A., Stryker, M. P., and Gandhi, S. P. (2010). Cortical plasticity induced by inhibitory neuron transplantation. Science 327, 1145-1148. doi: 10.1126/science.1183962
92. Spencer, C. M., Alekseyenko, O., Serysheva, E., Yuva-Paylor, L. A., and Paylor, R. (2005). Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Genes Brain Behav. 4, 420-430. doi: 10.1111/j.1601-183X.2005.00123.x
93. Sugiyama, S., Di Nardo, A. A., Aizawa, S., Matsuo, I., Volovitch, M., Prochiantz, A., et al. (2008). Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 134, 508-520. doi: 10.1016/j.cell. 2008.05.054
94. Sybirska, E., Davachi, L., and Goldman-Rakic, P. S. (2000). Prominence of direct entorhinal-CA1 pathway activation in sensorimotor and cognitive tasks revealed by 2-DG functional mapping in nonhuman primate. J. Neurosci. 20, 5827-5834.
95. Verkerk, A. J., Pieretti, M., Sutcliffe, J. S., Fu, Y. H., Kuhl, D. P., Pizzuti, A., et al. (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. doi: 10.1016/0092-8674(91)90397-H
96. Voineagu, I., Wang, X., Johnston, P., Lowe, J. K., Tian, Y., Horvath, S., et al. (2011). Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 474, 380-384. doi: 10.1038/nature10110
97. Wang, H., Chan, S. A., Ogier, M., Hellard, D., Wang, Q., Smith, C., et al. (2006). Dysregulation of brain-derived neurotrophic factor expression and neurosecretory function in Mecp2 null mice. J. Neurosci. 26, 10911-10915. doi: 10.1523/JNEUROSCI.1810-06.2006
98. Wiesel, T. N., and Hubel, D. H. (1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003-1017
99. Zhang, Z. W., Zak, J. D., and Liu, H. (2010). MeCP2 is required for normal development of GABAergic circuits in the thalamus. J. Neurophysiol. 103, 2470-2481. doi: 10.1152/jn.00601.2009
100. Zhou, Z., Hong, E. J., Cohen, S., Zhao, W. N., Ho, H. Y., Schmidt, L., et al. (2006). Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255-269. doi: 10.1016/j.neuron.2006.09.037