Activity-dependent adaptations in inhibitory axons

Frontiers in Cellular Neuroscience

Volumn 7, Issue NOV, 2013, Pages

  Frias, Cátia P ^a   Wierenga, Corette J ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Axons; Cell adhesion molecules; GABAergic synapses; Homeostatic plasticity; Interneurons

Indexed keywords

4 AMINOBUTYRIC ACID; BRAIN DERIVED NEUROTROPHIC FACTOR; CELL ADHESION MOLECULE; FIBROBLAST GROWTH FACTOR; NEU DIFFERENTIATION FACTOR; NEUROLIGIN; PROTEIN; SECRETORY PROTEIN; SEMAPHORIN; SLITRK3 PROTEIN; UNCLASSIFIED DRUG;

ADAPTATION; CELL ADHESION; CELLULAR DISTRIBUTION; GLIA CELL; HUMAN; NERVE CONDUCTION; NERVE FIBER; NONHUMAN; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN INTERACTION; REVIEW; RNA SPLICING; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTOSOME;

EID: 84888426232     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2013.00219     Document Type: Review

References (241)

1. Ango, F., di Cristo, G., Higashiyama, H., Bennett, V., Wu, P., and Huang, Z. J. (2004). Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119, 257-272. doi: 10.1016/j.cell.2004.10.004.
2. Aoto, J., Martinelli, D. C., Malenka, R. C., Tabuchi, K., and Südhof, T. C. (2013). Presynaptic neurexin-3 alternative splicing trans-synaptically controls postsynaptic AMPA receptor trafficking. Cell 154, 75-88. doi: 10.1016/j.cell.2013.05.060.
3. Aruga, J., and Mikoshiba, K. (2003). Identification and characterization of Slitrk, a novel neuronal transmembrane protein family controlling neurite outgrowth. Mol. Cell. Neurosci. 24, 117-129. doi: 10.1016/S1044-7431(03)00129-5.
4. Ascoli, G. A., Alonso-Nanclares, L., Anderson, S. A., Barrionuevo, G., Benavides-Piccione, R., Burkhalter, A., et al. (2008). Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557-568. doi: 10.1038/nrn2402.
5. Bamji, S. X., Rico, B., Kimes, N., and Reichardt, L. F. (2006). BDNF mobilizes synaptic vesicles and enhances synapse formation by disrupting cadherin-beta-catenin interactions. J. Cell Biol. 174, 289-299. doi: 10.1083/jcb.200601087.
6. Bamji, S. X., Shimazu, K., Kimes, N., Huelsken, J., Birchmeier, W., Lu, B., et al. (2003). Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 40, 719-731. doi: 10.1016/S0896-6273(03)00718-9.
7. Bartley, A. F., Huang, Z. J., Huber, K. M., and Gibson, J. R. (2008). Differential activity-dependent, homeostatic plasticity of two neocortical inhibitory circuits. J. Neurophysiol. 100, 1983-1994. doi: 10.1152/jn.90635.2008.
8. Basile, J. R., Barac, A., Zhu, T., Guan, K.-L., and Gutkind, J. S. (2004). Class IV semaphorins promote angiogenesis by stimulating Rho-initiated pathways through plexin-B. Cancer Res. 64, 5212-5224. doi: 10.1158/0008-5472.CAN-04-0126.
9. Basile, J. R., Holmbeck, K., Bugge, T. H., and Gutkind, J. S. (2007). MT1-MMP controls tumor-induced angiogenesis through the release of semaphorin 4D. J. Biol. Chem.282, 6899-6905. doi: 10.1074/jbc.M609570200.
10. Bateup, H. S., Johnson, C. A, Denefrio, C. L., Saulnier, J. L., Kornacker, K., and Sabatini, B. L. (2013). Excitatory/inhibitory synaptic imbalance leads to hippocampal hyperexcitability in mouse models of tuberous sclerosis. Neuron 78, 510-522. doi: 10.1016/j.neuron.2013.03.017.
11. Blundell, J., Tabuchi, K., Bolliger, M. F., Blaiss, C. A., Brose, N., Liu, X., et al. (2009). Increased anxiety-like behavior in mice lacking the inhibitory synapse cell adhesion molecule neuroligin 2. Genes. Brain. Behav. 8, 114-126. doi: 10.1111/j.1601-183X.2008. 00455.x.
12. Boyken, J., Grønborg, M., Riedel, D., Urlaub, H., Jahn, R., and Chua, J. J. E. (2013). Molecular profiling of synaptic vesicle docking sites reveals novel proteins but few differences between glutamatergic and GABAergic synapses. Neuron 78, 285-297. doi: 10.1016/j.neuron.2013.02.027.
13. Bragina, L., Fattorini, G., Giovedì, S., Bosco, F., Benfenati, F., and Conti, F. (2013). Heterogeneity of presynaptic proteins: do not forget isoforms. Front. Cell. Neurosci.7:8. doi: 10.3389/fncel.2013.00008.
14. Branco, T., Staras, K., Darcy, K. J., and Goda, Y. (2008). Local dendritic activity sets release probability at hippocampal synapses. Neuron 59, 475-485. doi: 10.1016/j.neuron.2008.07.006.
15. Brennaman, L. H., and Maness, P. F. (2008). Developmental regulation of GABAergic interneuron branching and synaptic development in the prefrontal cortex by soluble neural cell adhesion molecule. Mol. Cell. Neurosci. 37, 781-793. doi: 10.1016/j.mcn.2008.01.006.
16. Brennaman, L. H., Zhang, X., Guan, H., Triplett, J. W., Brown, A., Demyanenko, G. P., et al. (2013). Polysialylated NCAM and ephrinA/EphA regulate synaptic development of GABAergic interneurons in prefrontal cortex. Cereb. Cortex 23, 162-177. doi: 10.1093/cercor/bhr392.
17. Brenneke, F., Bukalo, O., Dityatev, A., and Lie, A. A. (2004). Mice deficient for the extracellular matrix glycoprotein tenascin-r show physiological and structural hallmarks of increased hippocampal excitability, but no increased susceptibility to seizures in the pilocarpine model of epilepsy. Neuroscience 124, 841-855. doi: 10.1016/j.neuroscience.2003.11.037.
18. Brünig, I., Suter, A., Knuesel, I., Lüscher, B., and Fritschy, J.-M. (2002). GABAergic terminals are required for postsynaptic clustering of dystrophin but not of GABA(A) receptors and gephyrin. J. Neurosci. 22, 4805-4813.
19. Buckby, L. E., Jensen, T. P., Smith, P. J. E., and Empson, R. M. (2006). Network stability through homeostatic scaling of excitatory and inhibitory synapses following inactivity in CA3 of rat organotypic hippocampal slice cultures. Mol. Cell. Neurosci.31, 805-816. doi: 10.1016/j.mcn.2006.01.009.
20. Bukalo, O., and Dityatev, A. (2012). Synaptic cell adhesion molecules. Adv. Exp. Med. Biol. 970, 97-128. doi: 10.1007/978-3-7091-0932-8_5.
21. Burkarth, N., Kriebel, M., Kranz, E. U., and Volkmer, H. (2007). Neurofascin regulates the formation of gephyrin clusters and their subsequent translocation to the axon hillock of hippocampal neurons. Mol. Cell. Neurosci. 36, 59-70. doi: 10.1016/j.mcn.2007.06.001.
22. Burrone, J., and Murthy, V. N. (2003). Synaptic gain control and homeostasis. Curr. Opin. Neurobiol. 13, 560-567. doi: 10.1016/j.conb.2003.09.007.
23. Bury, L. A., and Sabo, S. L. (2011). Coordinated trafficking of synaptic vesicle and active zone proteins prior to synapse formation. Neural Dev. 6, 24. doi: 10.1186/1749-8104-6-24.
24. Cai, Q., and Sheng, Z.-H. (2009). Mitochondrial transport and docking in axons. Exp. Neurol. 218, 257-267. doi: 10.1016/j.expneurol.2009.03.024.
25. Castillo, P. E., Chiu, C. Q., and Carroll, R. C. (2011). Long-term plasticity at inhibitory synapses. Curr. Opin. Neurobiol. 21, 328-338. doi: 10.1016/j.conb.2011.01.006.
26. Chan, C.-S., Weeber, E. J., Kurup, S., Sweatt, J. D., and Davis, R. L. (2003). Integrin requirement for hippocampal synaptic plasticity and spatial memory. J. Neurosci. 23, 7107-7116.
27. Charrier, C., Machado, P., Tweedie-Cullen, R. Y., Rutishauser, D., Mansuy, I. M., and Triller, A. (2010). A crosstalk between β1 and β3 integrins controls glycine receptor and gephyrin trafficking at synapses. Nat. Neurosci. 13, 1388-1395. doi: 10.1038/nn.2645.
28. Chattopadhyaya, B., Baho, E., Huang, Z. J., Schachner, M., and Di Cristo, G. (2013). Neural cell adhesion molecule-mediated Fyn activation promotes GABAergic synapse maturation in postnatal mouse cortex. J. Neurosci. 33, 5957-5968. doi: 10.1523/JNEUROSCI.1306-12.2013.
29. Chattopadhyaya, B., Cristo, G. Di, Higashiyama, H., Knott, G. W., Kuhlman, S. J., Welker, E., et al. (2004). Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci. 24, 9598-9611. doi: 10.1523/JNEUROSCI.1851-04.2004.
30. Chattopadhyaya, B., Di Cristo, G., Wu, C. Z., Knott, G., Kuhlman, S., Fu, Y., et al. (2007). GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 54, 889-903. doi: 10.1016/j.neuron.2007.05.015.
31. Chavis, P., and Westbrook, G. (2001). Integrins mediate functional pre-and postsynaptic maturation at a hippocampal synapse. Nature 411, 317-321. doi: 10.1038/35077101.
32. Chen, J. L., Lin, W. C., Cha, J. W., So, P. T., Kubota, Y., and Nedivi, E. (2011). Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat. Neurosci. 14, 587-594. doi: 10.1038/nn.2799.
33. Chen, J. L., Villa, K. L., Cha, J. W., So, P. T. C., Kubota, Y., and Nedivi, E. (2012). Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 74, 361-373. doi: 10.1016/j.neuron.2012.02.030.
34. Chia, P. H., Patel, M. R., and Shen, K. (2012). NAB-1 instructs synapse assembly by linking adhesion molecules and F-actin to active zone proteins. Nat. Neurosci. 15, 234-242. doi: 10.1038/nn.2991.
35. Chih, B., Gollan, L., and Scheiffele, P. (2006). Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51, 171-178. doi: 10.1016/j.neuron.2006.06.005.
36. Christopherson, K. S., Stokes, C. C. A., Barres, B. A., Ullian, E. M., Mullowney, C. E., Hell, J. W., et al. (2005a). Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120, 421-433. doi: 10.1016/j.cell.2004.12.020.
37. Christopherson, K. S., Ullian, E. M., Stokes, C. C. A., Mullowney, C. E., Hell, J. W., Agah, A., et al. (2005b). Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120, 421-433. doi: 10.1016/j.cell.2004.12.020.
38. Chubykin, A. A., Atasoy, D., Etherton, M. R., Brose, N., Kavalali, E. T., Gibson, J. R., et al. (2007). Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54, 919-931. doi: 10.1016/j.neuron.2007.05.029.
39. Cingolani, L. A., and Goda, Y. (2008). Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 9, 344-356. doi: 10.1038/nrn2373.
40. Cingolani, L. A., Thalhammer, A., Yu, L. M. Y., Catalano, M., Ramos, T., Colicos, M. A., et al. (2008). Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins. Neuron 58, 749-762. doi: 10.1016/j.neuron.2008.04.011.
41. Coggan, J. S., Bartol, T. M., Esquenazi, E., Stiles, J. R., Lamont, S., Martone, M. E., et al. (2005). Evidence for ectopic neurotransmission at a neuronal synapse. Science 309, 446-451. doi: 10.1126/science.1108239.
42. Crawford, D. C., Jiang, X., Taylor, A., and Mennerick, S. (2012). Astrocyte-derived thrombospondins mediate the development of hippocampal presynaptic plasticity in vitro. J. Neurosci. 32, 13100-13110. doi: 10.1523/JNEUROSCI.2604-12.2012.
43. Di Cristo, G., Chattopadhyaya, B., Kuhlman, S. J., Fu, Y., Bélanger, M.-C., Wu, C. Z., et al. (2007). Activity-dependent PSA expression regulates inhibitory maturation and onset of critical period plasticity. Nat. Neurosci. 10, 1569-1577. doi: 10.1038/nn2008.
44. Cristóvão-Ferreira, S., Vaz, S. H., Ribeiro, J. A, and Sebastião, A. M. (2009). Adenosine A2A receptors enhance GABA transport into nerve terminals by restraining PKC inhibition of GAT-1. J. Neurochem. 109, 336-347. doi: 10.1111/j.1471-4159.2009.05963.x.
45. Cunha, R. A, and Ribeiro, J. A. (2000). Purinergic modulation of [(3)H]GABA release from rat hippocampal nerve terminals. Neuropharmacology 39, 1156-1167. doi: 10.1016/S0028-3908(99)00237-3.
46. Dalva, M. B., McClelland, A. C., and Kayser, M. S. (2007). Cell adhesion molecules: signalling functions at the synapse. Nat. Rev. Neurosci. 8, 206-220. doi: 10.1038/nrn2075.
47. Darcy, K. J., Staras, K., Collinson, L. M., and Goda, Y. (2006). Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat. Neurosci. 9, 315-321. doi: 10.1038/nn1640.
48. delPino, I., García-Frigola, C., Dehorter, N., Brotons-Mas, J. R., Alvarez-Salvado, E., Martínez de Lagrán, M., et al. (2013). Erbb4 deletion from fast-spiking interneurons causes schizophrenia-like phenotypes. Neuron 79, 1152-1168. doi: 10.1016/j.neuron.2013.07.010.
49. Ding, J. B., Oh, W.-J., Sabatini, B. L., and Gu, C. (2012). Semaphorin 3E-Plexin-D1 signaling controls pathway-specific synapse formation in the striatum. Nat. Neurosci.15, 215-223. doi: 10.1038/nn.3003.
50. Dobie, F. A., and Craig, A. M. (2011). Inhibitory synapse dynamics: coordinated presynaptic and postsynaptic mobility and the major contribution of recycled vesicles to new synapse formation. J. Neurosci. 31, 10481-10493. doi: 10.1523/JNEUROSCI.6023-10.2011.
51. Dono, R. (2003). Fibroblast growth factors as regulators of central nervous system development and function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284, R867-R881. doi: 10.1152/ajpregu.00533.2002.
52. Echegoyen, J., Neu, A., Graber, K. D., and Soltesz, I. (2007). Homeostatic plasticity studied using in vivo hippocampal activity-blockade: synaptic scaling, intrinsic plasticity and age-dependence. PLoS ONE 2:e700. doi:10.1371/journal.pone.0000700.
53. Elmariah, S. B., Oh, E. J., Hughes, E. G., and Balice-Gordon, R. J. (2005). Astrocytes regulate inhibitory synapse formation via Trk-mediated modulation of postsynaptic GABAA receptors. J. Neurosci. 25, 3638-3635. doi: 10.1523/JNEUROSCI.3980-04.2005.
54. Eroglu, C., O'Rourke, N. A., Barres, B. A., Allen, N. J., Susman, M. W., Park, C. Y., et al. (2009). Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139, 380-392. doi: 10.1016/j.cell.2009.09.025.
55. Fazzari, P., Paternain, A. V, Valiente, M., Pla, R., Luján, R., Lloyd, K., et al. (2010). Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature464, 1376-1380. doi: 10.1038/nature08928.
56. Fernández-Busnadiego, R., Zuber, B., Maurer, U. E., Cyrklaff, M., Baumeister, W., and Lucic, V. (2010). Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography. J. Cell Biol. 188, 145-156. doi: 10.1083/jcb.200908082.
57. Fisher-Lavie, A., Zeidan, A., Stern, M., Garner, C. C., and Ziv, N. E. (2011). Use dependence of presynaptic tenacity. J. Neurosci. 31, 16770-16780. doi: 10.1523/JNEUROSCI.3384-11.2011.
58. Fisher-Lavie, A., and Ziv, N. E. (2013). Matching dynamics of presynaptic and postsynaptic scaffolds. J. Neurosci. 33, 13094-13100. doi: 10.1523/JNEUROSCI.2144-13.2013.
59. Flajolet, M., Wang, Z., Futter, M., Shen, W., Nuangchamnong, N., Bendor, J., et al. (2008). FGF acts as a co-transmitter through adenosine A(2A) receptor to regulate synaptic plasticity. Nat. Neurosci. 11, 1402-1409. doi: 10.1038/nn.2216.
60. Friedman, H. V, Bresler, T., Garner, C. C., and Ziv, N. E. (2000). Assembly of new individual excitatory synapses: time course and temporal order of synaptic molecule recruitment. Neuron 27, 57-69. doi: 10.1016/S0896-6273(00)00009-X.
61. Frischknecht, R., Fejtova, A., Viesti, M., Stephan, A., and Sonderegger, P. (2008). Activity-induced synaptic capture and exocytosis of the neuronal serine protease neurotrypsin. Cultures 28, 1568-1579. doi: 10.1523/JNEUROSCI.3398-07.2008.
62. Fu, Y., and Huang, Z. J. (2010). Differential dynamics and activity-dependent regulation of α-and β-neurexins at developing GABAergic synapses. Proc. Natl. Acad. Sci. U.S.A. 107, 22699-22704. doi: 10.1073/pnas.1011233108.
63. Fu, Y., Wu, X., Lu, J., and Huang, Z. J. (2012). Presynaptic GABAB receptor regulates activity-dependent maturation and patterning of inhibitory synapses through dynamic allocation of synaptic vesicles. Front. Cell. Neurosci. 6:57. doi: 10.3389/fncel.2012.00057.
64. Fukaya, M., Kamata, A., Hara, Y., Tamaki, H., Katsumata, O., Ito, N., et al. (2011). SynArfGEF is a guanine nucleotide exchange factor for Arf6 and localizes preferentially at post-synaptic specializations of inhibitory synapses. J. Neurochem.116, 1122-1137. doi: 10.1111/j.1471-4159.2010.07167.x.
65. Futai, K., Doty, C. D., Baek, B., Ryu, J., and Sheng, M. (2013). Specific trans-synaptic interaction with inhibitory interneuronal neurexin underlies differential ability of neuroligins to induce functional inhibitory synapses. J. Neurosci. 33, 3612-3623. doi: 10.1523/JNEUROSCI.1811-12.2013.
66. Gambino, F., and Holtmaat, A. (2012). Spike-timing-dependent potentiation of sensory surround in the somatosensory cortex is facilitated by deprivation-mediated disinhibition. Neuron 75, 490-502. doi: 10.1016/j.neuron.2012.05.020.
67. Gibson, J. R., Huber, K. M., and Südhof, T. C. (2009). Neuroligin-2 deletion selectively decreases inhibitory synaptic transmission originating from fast-spiking but not from somatostatin-positive interneurons. Cell 29, 13883-13897. doi: 10.1523/JNEUROSCI.2457-09.2009.
68. Gitler, D., Takagishi, Y., Feng, J., Ren, Y., Rodriguiz, R. M., Wetsel, W. C., et al. (2004). Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J. Neurosci. 24, 11368-11380. doi: 10.1523/JNEUROSCI.3795-04.2004.
69. De Gois, S., Schäfer, M. K.-H., Defamie, N., Chen, C., Ricci, A., Weihe, E., et al. (2005). Homeostatic scaling of vesicular glutamate and GABA transporter expression in rat neocortical circuits. J. Neurosci. 25, 7121-7133. doi: 10.1523/JNEUROSCI.5221-04.2005.
70. Goldstein, A. Y. N., Wang, X., and Schwarz, T. L. (2008). Axonal transport and the delivery of pre-synaptic components. Curr. Opin. Neurobiol. 18, 495-503. doi: 10.1016/j.conb.2008.10.003.
71. Gottmann, K., Lessmann, V., and Mittmann, T. (2009). BDNF signaling in the formation, maturation and plasticity of glutamatergic and GABAergic synapses. Exp. Brain Res. 199, 203-234. doi: 10.1007/s00221-009-1994-z.
72. Grady, R. M., Wozniak, D. F., Ohlemiller, K. K., and Sanes, J. R. (2006). Cerebellar synaptic defects and abnormal motor behavior in mice lacking alpha-and beta-dystrobrevin. J. Neurosci. 26, 2841-2851. doi: 10.1523/JNEUROSCI.4823-05.2006.
73. Graf, E. R., Kang, Y., Hauner, A. M., and Craig, A. M. (2006). Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J. Neurosci. 26, 4256-4265. doi: 10.1523/JNEUROSCI.1253-05.2006.
74. Graf, E. R., Zhang, X., Jin, S. X., Linhoff, M. W., and Craig, A. M. (2004). Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119, 1013-1026. doi: 10.1016/j.cell.2004.11.035.
75. Grønborg, M., Pavlos, N. J., Brunk, I., Chua, J. J. E., Münster-Wandowski, A., Riedel, D., et al. (2010). Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein. J. Neurosci. 30, 2-12. doi: 10.1523/JNEUROSCI.4074-09.2010.
76. Guillaud, L., Wong, R., and Hirokawa, N. (2008). Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: a molecular model of kinesin-cargo release. Nat. Cell Biol. 10, 19-29. doi: 10.1038/ncb1665.
77. Han, S., Tai, C., Westenbroek, R. E., Yu, F. H., Cheah, C. S., Potter, G. B., et al. (2012). Autistic-like behaviour in Scn1a± mice and rescue by enhanced GABA-mediated neurotransmission. Nature 489, 385-390. doi: 10.1038/nature11356.
78. Harburger, D. S., and Calderwood, D. A. (2009). Integrin signalling at a glance. J. Cell Sci. 122, 159-163. doi: 10.1242/jcs.018093.
79. Harms, K. J., and Craig, A. M. (2005). Synapse composition and organization following chronic activity blockade in cultured hippocampal neurons. J. Comp. Neurol. 490, 72-84. doi: 10.1002/cne.20635.
80. Hartman, K. N., Pal, S. K., Burrone, J., and Murthy, V. N. (2006). Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. Nat. Neurosci. 9, 642-649. doi: 10.1038/nn1677.
81. Hattori, D., Millard, S. S., Wojtowicz, W. M., and Zipursky, S. L. (2008). Dscam-mediated cell recognition regulates neural circuit formation. Annu. Rev. Cell Dev. Biol. 24, 597-620. doi: 10.1146/annurev.cellbio.24.110707.175250.
82. Heifets, B. D., and Castillo, P. E. (2009). Endocannabinoid signaling and long-term synaptic plasticity. Annu. Rev. Physiol. 71, 283-306. doi: 10.1146/annurev.physiol.010908.163149.
83. Hensch, T. K. (2005). Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877-888. doi: 10.1038/nrn1787.
84. Huang, Z. J. (2009). Activity-dependent development of inhibitory synapses and innervation pattern: role of GABA signalling and beyond. J. Physiol. 587, 1881-1888. doi: 10.1113/jphysiol.2008.168211.
85. 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.
86. Huang, Z. J., and Scheiffele, P. (2008). GABA and neuroligin signaling: linking synaptic activity and adhesion in inhibitory synapse development. Curr. Opin. Neurobiol. 18, 77-83. doi: 10.1016/j.conb.2008.05.008.
87. Hughes, E. G., Elmariah, S. B., and Balice-Gordon, R. J. (2010). Astrocyte secreted proteins selectively increase hippocampal GABAergic axon length, branching, and synaptogenesis. Mol. Cell. Neurosci. 43, 136-145. doi: 10.1016/j.mcn.2009.10.004.
88. Hynes, R. O. (2002). Integrins?: bidirectional, allosteric signaling machines. Cell 110, 673-687. doi: 10.1016/S0092-8674(02)00971-6.
89. Jedlicka, P., Hoon, M., Papadopoulos, T., Vlachos, A., Winkels, R., Poulopoulos, A., et al. (2011). Increased dentate gyrus excitability in neuroligin-2-deficient mice in vivo. Cereb. Cortex 21, 357-367. doi: 10.1093/cercor/bhq100.
90. Jiang, X., Wang, G., Lee, A. J., Stornetta, R. L., and Zhu, J. J. (2013). The organization of two new cortical interneuronal circuits. Nat. Neurosci. 16, 210-220. doi: 10.1038/nn.3305.
91. Jin, Y., and Garner, C. C. (2008). Molecular mechanisms of presynaptic differentiation. Annu. Rev. Cell Dev. Biol. 24, 237-262. doi: 10.1146/annurev.cellbio.23.090506.123417.
92. Kaeser, P. S., Deng, L., Chávez, A. E., Liu, X., Castillo, P. E., and Südhof, T. C. (2009). ELKS2alpha/CAST deletion selectively increases neurotransmitter release at inhibitory synapses. Neuron 64, 227-239. doi: 10.1016/j.neuron.2009.09.019.
93. Kang, Y., Zhang, X., Dobie, F., Wu, H., and Craig, A. M. (2008). Induction of GABAergic postsynaptic differentiation by alpha-neurexins. J. Biol. Chem. 283, 2323-2334. doi: 10.1074/jbc.M703957200.
94. Karmarkar, U. R., and Buonomano, D. V (2006). Different forms of homeostatic plasticity are engaged with distinct temporal profiles. Eur. J. Neurosci. 23, 1575-1584. doi: 10.1111/j.1460-9568.2006.04692.x.
95. Keck, T., Scheuss, V., Jacobsen, R. I. I., Wierenga, C. J. J., Eysel, U. T. T., Bonhoeffer, T., et al. (2011). Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 71, 869-882. doi: 10.1016/j.neuron.2011.06.034.
96. Kerr, A. M., Reisinger, E., and Jonas, P. (2008). Differential dependence of phasic transmitter release on synaptotagmin 1 at GABAergic and glutamatergic hippocampal synapses. Proc. Natl. Acad. Sci. U.S.A. 105, 15581-15586. doi: 10.1073/pnas.0800621105.
97. Kilman, V., Van Rossum, M. C., and Turrigiano, G. G. (2002). Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABA. J. Neurosci. 22, 1328-1337.
98. Kim, C., Ye, F., and Ginsberg, M. H. (2011a). Regulation of integrin activation. Annu. Rev. Cell Dev. Biol. 27, 321-345. doi: 10.1146/annurev-cellbio-100109-104104.
99. Kim, J., and Alger, B. E. (2010). Reduction in endocannabinoid tone is a homeostatic mechanism for specific inhibitory synapses. Nat. Neurosci. 13, 592-600. doi: 10.1038/nn.2517.
100. Kim, S. A., Tai, C.-Y., Mok, L.-P., Mosser, E. A., and Schuman, E. M. (2011b). Calcium-dependent dynamics of cadherin interactions at cell-cell junctions. Proc. Natl. Acad. Sci. U.S.A. 108, 9857-9862. doi: 10.1073/pnas.1019003108.
101. Kim, S. H., and Ryan, T. A. (2013). Balance of calcineurin A and CDK5 activities sets release probability at nerve terminals. J. Neurosci. 33, 8937-8950. doi: 10.1523/JNEUROSCI.4288-12.2013.
102. Kim, S. H., and Ryan, T. A. (2010). CDK5 serves as a major control point in neurotransmitter release. Neuron 67, 797-809. doi: 10.1016/j.neuron.2010.08.003.
103. Klausberger, T., and Somogyi, P. (2008). Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53-57. doi: 10.1126/science.1149381.
104. Knuesel, I., Mastrocola, M., Zuellig, R. A., Bornhauser, B., Schaub, M. C., and Fritschy, J. (1999). Altered synaptic clustering of GABA A receptors in mice lacking dystrophin (mdx mice). Eur. J. Neurosci. 11, 4457-4462. doi: 10.1046/j.1460-9568.1999.00887.x.
105. Ko, J., Soler-Llavina, G. J., Fuccillo, M. V, Malenka, R. C., and Südhof, T. C. (2011). Neuroligins/LRRTMs prevent activity-and Ca2+/calmodulin-dependent synapse elimination in cultured neurons. J. Cell Biol. 194, 323-334. doi: 10.1083/jcb.201101072.
106. 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 brain-derived neurotrophic factor, as revealed by single-cell gene knock-out method. J. Neurosci. 27, 7234-7244. doi: 10.1523/JNEUROSCI.1943-07.2007.
107. Kolarow, R., Brigadski, T., and Lessmann, V. (2007). Postsynaptic secretion of BDNF and NT-3 from hippocampal neurons depends on calcium calmodulin kinase II signaling and proceeds via delayed fusion pore opening. J. Neurosci. 27, 10350-10364. doi: 10.1523/JNEUROSCI.0692-07.2007.
108. Kriebel, M., Metzger, J., Trinks, S., Chugh, D., Harvey, R. J., Harvey, K., et al. (2011). The cell adhesion molecule neurofascin stabilizes axo-axonic GABAergic terminals at the axon initial segment. J. Biol. Chem. 286, 24385-24393. doi: 10.1074/jbc.M110.212191.
109. Krueger, D. D., Tuffy, L. P., Papadopoulos, T., and Brose, N. (2012). The role of neurexins and neuroligins in the formation, maturation, and function of vertebrate synapses. Curr. Opin. Neurobiol. 22, 412-422. doi: 10.1016/j.conb.2012.02.012.
110. Krueger, S. R., Kolar, A., and Fitzsimonds, R. M. (2003). The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron 40, 945-957. doi: 10.1016/S0896-6273(03)00729-3.
111. Kubota, K., Inoue, K., Hashimoto, R., Kumamoto, N., Kosuga, A., Tatsumi, M., et al. (2009). Tumor necrosis factor receptor-associated protein 1 regulates cell adhesion and synaptic morphology via modulation of N-cadherin expression. J. Neurochem.110, 496-508. doi: 10.1111/j.1471-4159.2009.06099.x.
112. Kuczewski, N., Porcher, C., Ferrand, N., Pellegrino, C., Kolarow, R., Lessmann, V., et al. (2008). Backpropagating action potentials trigger dendritic release of BDNF during spontaneous network activity. J. Neurosci. 28, 7013-7023. doi: 10.1523/JNEUROSCI.1673-08.2008.
113. Kuhlman, S. J., and Huang, Z. J. (2008). High-resolution labeling and functional manipulation of specific neuron types in mouse brain by Cre-activated viral gene expression. PLoS ONE 3:e2005. doi: 10.1371/journal.pone.0002005.
114. Kuriu, T., Yanagawa, Y., and Konishi, S. (2012). Activity-dependent coordinated mobility of hippocampal inhibitory synapses visualized with presynaptic and postsynaptic tagged-molecular markers. Mol. Cell. Neurosci. 49, 184-195. doi: 10.1016/j.mcn.2011.11.002.
115. Kuzirian, M. S., Moore, A. R., Staudenmaier, E. K., Friedel, R. H., and Paradis, S. (2013). The class 4 semaphorin sema4D promotes the rapid assembly of GABaergic synapses in rodent hippocampus. J. Neurosci. 33, 8961-8973. doi: 10.1523/JNEUROSCI.0989-13.2013.
116. Lau, C. G., and Murthy, V. N. (2012). Activity-dependent regulation of inhibition via GAD67. J. Neurosci. 32, 8521-8531. doi: 10.1523/JNEUROSCI.1245-12.2012.
117. Lee, K., Kim, Y., Lee, S.-J., Qiang, Y., Lee, D., Lee, H. W., et al. (2013). MDGAs interact selectively with neuroligin-2 but not other neuroligins to regulate inhibitory synapse development. Proc. Natl. Acad. Sci. U.S.A. 110, 336-341. doi: 10.1073/pnas.1219987110.
118. Lévi, S., Grady, R. M., Henry, M. D., Campbell, K. P., Sanes, J. R., and Craig, A. M. (2002). Dystroglycan is selectively associated with inhibitory GABAergic synapses but is dispensable for their differentiation. J. Neurosci. 22, 4274-4285.
119. Li, R.-W., Yu, W., Christie, S., Miralles, C. P., Bai, J., Loturco, J. J., et al. (2005). Disruption of postsynaptic GABA receptor clusters leads to decreased GABAergic innervation of pyramidal neurons. J. Neurochem. 95, 756-770. doi: 10.1111/j.1471-4159.2005.03426.x.
120. Linhoff, M. W., Laurén, J., Cassidy, R. M., Dobie, F. A., Takahashi, H., Nygaard, H. B., et al. (2009). An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron 61, 734-749. doi: 10.1016/j.neuron.2009.01.017.
121. Liu, Y., Zhang, L. I., and Tao, H. W. (2007). Heterosynaptic scaling of developing GABAergic synapses: dependence on glutamatergic input and developmental stage. J. Neurosci. 27, 5301-5312. doi: 10.1523/JNEUROSCI.0376-07.2007.
122. Maas, C., Belgardt, D., Lee, H. K., Heisler, F. F., Lappe-Siefke, C., Magiera, M. M., et al. (2009). Synaptic activation modifies microtubules underlying transport of postsynaptic cargo. Proc. Natl. Acad. Sci. U.S.A. 106, 8731-8736. doi: 10.1073/pnas.0812391106.
123. MacAskill, A. F., Rinholm, J. E., Twelvetrees, A. E., Arancibia-Carcamo, I. L., Muir, J., Fransson, A., et al. (2009). Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 61, 541-555. doi: 10.1016/j.neuron.2009.01.030.
124. Maffei, A., Lambo, M. E., and Turrigiano, G. G. (2010). Critical period for inhibitory plasticity in rodent binocular V1. J. Neurosci. 30, 3304-3309. doi: 10.1523/JNEUROSCI.5340-09.2010.
125. Maffei, A., Nataraj, K., Nelson, S. B., and Turrigiano, G. G. (2006). Potentiation of cortical inhibition by visual deprivation. Nature 443, 81-84. doi: 10.1038/nature05079.
126. Maffei, A., Nelson, S. B., and Turrigiano, G. G. (2004). Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat. Neurosci. 7, 1353-1359. doi: 10.1038/nn1351.
127. Maffei, A., and Turrigiano, G. G. (2008). Multiple modes of network homeostasis in visual cortical layer 2/3. J. Neurosci. 28, 4377-4384. doi: 10.1523/JNEUROSCI.5298-07.2008.
128. Marik, S. A, Yamahachi, H., McManus, J. N. J., Szabo, G., and Gilbert, C. D. (2010). Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLoS Biol. 8:e1000395. doi: 10.1371/journal.pbio.1000395.
129. Marty, S., Wehrlé, R., Fritschy, J., and Sotelo, C. (2004). Quantitative effects produced by modifications of neuronal activity on the size of GABA A receptor clusters in hippocampal slice cultures. Eur. J. Neurosci. 20, 427-440. doi: 10.1111/j.1460-9568.2004.03491.x.
130. 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.
131. Matsuda, N., Lu, H., Fukata, Y., Noritake, J., Gao, H., Mukherjee, S., et al. (2009). Differential activity-dependent secretion of brain-derived neurotrophic factor from axon and dendrite. J. Neurosci. 29, 14185-14198. doi: 10.1523/JNEUROSCI.1863-09.2009.
132. Matsumoto-Miyai, K., Sokolowska, E., Zurlinden, A., Gee, C. E., Lüscher, D., Hettwer, S., et al. (2009). Coincident pre-and postsynaptic activation induces dendritic filopodia via neurotrypsin-dependent agrin cleavage. Cell 136, 1161-1171. doi: 10.1016/j.cell.2009.02.034.
133. Mei, L., and Xiong, W.-C. (2008). Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat. Rev. Neurosci. 9, 437-452. doi: 10.1038/nrn2392.
134. Meijers, R., Puettmann-Holgado, R., Skiniotis, G., Liu, J., Walz, T., Wang, J., et al. (2007). Structural basis of Dscam isoform specificity. Nature 449, 487-491. doi: 10.1038/nature06147.
135. Missler, M., and Südhof, T. C. (1998). Neurexins: three genes and 1001 products. Trends Genet. 14, 20-26. doi: 10.1016/S0168-9525(97)01324-3.
136. Mizumoto, K., and Shen, K. (2013). Interaxonal interaction defines tiled presynaptic innervation in C. elegans. Neuron 77, 655-666. doi: 10.1016/j.neuron.2012.12.031.
137. Morita, A., Yamashita, N., Sasaki, Y., Uchida, Y., Nakajima, O., Nakamura, F., et al. (2006). Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. J. Neurosci. 26, 2971-2980. doi: 10.1523/JNEUROSCI.5453-05.2006.
138. Nikonenko, A., Schmidt, S., Skibo, G., Brückner, G., and Schachner, M. (2003). Tenascin-R-deficient mice show structural alterations of symmetric perisomatic synapses in the CA1 region of the hippocampus. J. Comp. Neurol. 456, 338-349. doi: 10.1002/cne.10537.
139. O'Connor, T. P., Cockburn, K., Wang, W., Tapia, L., Currie, E., and Bamji, S. X. (2009). Semaphorin 5B mediates synapse elimination in hippocampal neurons. Neural Dev. 4, 18. doi: 10.1186/1749-8104-4-18.
140. Obashi, K., and Okabe, S. (2013). Regulation of mitochondrial dynamics and distribution by synapse position and neuronal activity in the axon. Eur. J. Neurosci.38, 2350-2363. doi: 10.1111/ejn.12263.
141. Ohba, S., Ikeda, T., Ikegaya, Y., Nishiyama, N., Matsuki, N., and Yamada, M. K. (2005). BDNF locally potentiates GABAergic presynaptic machineries: target-selective circuit inhibition. Cereb. Cortex 15, 291-298. doi: 10.1093/cercor/bhh130.
142. Ormond, J., and Woodin, M. A. (2011). Disinhibition-mediated LTP in the hippocampus is synapse specific. Front. Cell. Neurosci. 5:17. doi: 10.3389/fncel.2011.00017.
143. Ou, C.-Y., and Shen, K. (2010). Setting up presynaptic structures at specific positions. Curr. Opin. Neurobiol. 20, 489-493. doi: 10.1016/j.conb.2010.04.011.
144. Owald, D., and Sigrist, S. J. (2009). Assembling the presynaptic active zone. Curr. Opin. Neurobiol. 19, 311-318. doi: 10.1016/j.conb.2009.03.003.
145. Palop, J. J., Chin, J., Roberson, E. D., Wang, J., Thwin, M. T., Bien-Ly, N., et al. (2007). Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55, 697-711. doi: 10.1016/j.neuron.2007.07.025.
146. Paradis, S., Harrar, D. B., Lin, Y., Koon, A. C., Hauser, J. L., Griffith, E. C., et al. (2007). An RNAi-based approach identifies molecules required for glutamatergic and GABAergic synapse development. Neuron 53, 217-232. doi: 10.1016/j.neuron.2006.12.012.
147. Park, H., and Poo, M. (2013). Neurotrophin regulation of neural circuit development and function. Nat. Rev. Neurosci. 14, 7-23. doi: 10.1038/nrn3379.
148. Pasterkamp, R. J. (2012). Getting neural circuits into shape with semaphorins. Nat. Rev. Neurosci. 13, 605-618. doi: 10.1038/nrn3302.
149. Patrizi, A., Scelfo, B., Viltono, L., Briatore, F., Fukaya, M., Watanabe, M., et al. (2008). Synapse formation and clustering of neuroligin-2 in the absence of GABAA receptors. Proc. Natl. Acad. Sci. U.S.A. 105, 13151-13156. doi: 10.1073/pnas.0802390105.
150. Pavlov, I., Rauvala, H., and Taira, T. (2006). Enhanced hippocampal GABAergic inhibition in mice overexpressing heparin-binding growth-associated molecule. Neuroscience 139, 505-511. doi: 10.1016/j.neuroscience.2005.11.070.
151. Peixoto, R. T., Kunz, P. A., Kwon, H., Mabb, A. M., Sabatini, B. L., Philpot, B. D., et al. (2012). Transsynaptic signaling by activity-dependent cleavage of neuroligin-1. Neuron 76, 396-409. doi: 10.1016/j.neuron.2012.07.006.
152. Peng, A., Rotman, Z., Deng, P.-Y., and Klyachko, V. A. (2012). Differential motion dynamics of synaptic vesicles undergoing spontaneous and activity-evoked endocytosis. Neuron 73, 1108-1115. doi: 10.1016/j.neuron.2012.01.023.
153. Peng, Y.-R., Zeng, S.-Y., Song, H.-L., Li, M.-Y., Yamada, M. K., and Yu, X. (2010). Postsynaptic spiking homeostatically induces cell-autonomous regulation of inhibitory inputs via retrograde signaling. J. Neurosci. 30, 16220-16231. doi: 10.1523/JNEUROSCI.3085-10.2010.
154. Pettem, K. L., Yokomaku, D., Takahashi, H., Ge, Y., and Craig, A. M. (2013). Interaction between autism-linked MDGAs and neuroligins suppresses inhibitory synapse development. J. Cell Biol. 200, 321-326. doi: 10.1083/jcb.201206028.
155. Pfeffer, C. K., Xue, M., He, M., Huang, Z. J., and Scanziani, M. (2013). Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16, 1068-1076. doi: 10.1038/nn.3446.
156. Pillai-Nair, N., Panicker, A. K., Rodriguiz, R. M., Gilmore, K. L., Demyanenko, G. P., Huang, J. Z., et al. (2005). Neural cell adhesion molecule-secreting transgenic mice display abnormalities in GABAergic interneurons and alterations in behavior. J. Neurosci. 25, 4659-4657. doi: 10.1523/JNEUROSCI.0565-05.2005.
157. Pinkstaff, J. K., Lynch, G., and Gall, C. M. (1998). Localization and seizure-regulation of integrin beta 1 mRNA in adult rat brain. Brain Res. Mol. Brain Res. 55, 265-276. doi: 10.1016/S0169-328X(98)00007-2.
158. Poulopoulos, A., Aramuni, G., Meyer, G., Soykan, T., Hoon, M., Harvey, K., et al. (2009). Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63, 628-642. doi: 10.1016/j.neuron.2009.08.023.
159. Pozo, K., and Goda, Y. (2010). Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66, 337-351. doi: 10.1016/j.neuron.2010.04.028.
160. Pregno, G., Frola, E., Graziano, S., Patrizi, A., Bussolino, F., Arese, M., et al. (2013). Differential regulation of neurexin at glutamatergic and GABAergic synapses. Front. Cell. Neurosci. 7:35. doi: 10.3389/fncel.2013.00035.
161. Raissi, A. J., Staudenmaier, E. K., David, S., Hu, L., and Paradis, S. (2013). Sema4D localizes to synapses and regulates GABAergic synapse development as a membrane-bound molecule in the mammalian hippocampus. Mol. Cell. Neurosci. 57C, 23-32. doi: 10.1016/j.mcn.2013.08.004.
162. Rannals, M. D., and Kapur, J. (2011). Homeostatic strengthening of inhibitory synapses is mediated by the accumulation of GABAA receptors. J. Neurosci. 31, 17701-17712. doi: 10.1523/JNEUROSCI.4476-11.2011.
163. Ratnayaka, A., Marra, V., Branco, T., and Staras, K. (2011). Extrasynaptic vesicle recycling in mature hippocampal neurons. Nat. Commun. 2, 531. doi: 10.1038/ncomms1534.
164. Regehr, W. G., Carey, M. R., and Best, A. R. (2009). Activity-dependent regulation of synapses by retrograde messengers. Neuron 63, 154-170. doi: 10.1016/j.neuron.2009.06.021.
165. Reuss, B., and von Bohlen und Halbach, O. (2003). Fibroblast growth factors and their receptors in the central nervous system. Cell Tissue Res. 313, 139-157. doi: 10.1007/s00441-003-0756-7.
166. Rose, T., Schoenenberger, P., Jezek, K., and Oertner, T. G. (2013). Developmental refinement of vesicle cycling at Schaffer collateral synapses. Neuron 77, 1109-1121. doi: 10.1016/j.neuron.2013.01.021.
167. Sabo, S. L., Gomes, R. A., and McAllister, A. K. (2006). Formation of presynaptic terminals at predefined sites along axons. J. Neurosci. 26, 10813-10825. doi: 10.1523/JNEUROSCI.2052-06.2006.
168. Saghatelyan, A. K., Dityatev, A., Schmidt, S., Schuster, T., Bartsch, U., and Schachner, M. (2001). Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol. Cell. Neurosci. 17, 226-240. doi: 10.1006/mcne.2000.0922.
169. Sahay, A., Kim, C.-H., Sepkuty, J. P., Cho, E., Huganir, R. L., Ginty, D. D., et al. (2005). Secreted semaphorins modulate synaptic transmission in the adult hippocampus. J. Neurosci. 25, 3613-3620. doi: 10.1523/JNEUROSCI.5255-04.2005.
170. Saliba, R. S., Michels, G., Jacob, T. C., Pangalos, M. N., and Moss, S. J. (2007). Activity-dependent ubiquitination of GABA(A) receptors regulates their accumulation at synaptic sites. J. Neurosci. 27, 13341-13351. doi: 10.1523/JNEUROSCI.3277-07.2007.
171. Sassoè-Pognetto, M., Frola, E., Pregno, G., Briatore, F., and Patrizi, A. (2011). Understanding the molecular diversity of GABAergic synapses. Front. Cell. Neurosci.5:4. doi: 10.3389/fncel.2011.00004.
172. Scheiffele, P., Fan, J., Choih, J., Fetter, R., and Serafini, T. (2000). Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell 101, 657-669. doi: 10.1016/S0092-8674(00)80877-6.
173. Schubert, T., Hoon, M., Euler, T., Lukasiewicz, P. D., and Wong, R. O. L. (2013). Developmental regulation and activity-dependent maintenance of GABAergic presynaptic inhibition onto rod bipolar cell axonal terminals. Neuron 78, 124-137. doi: 10.1016/j.neuron.2013.01.037.
174. Schuemann, A., Klawiter, A., Bonhoeffer, T., Wierenga, C. J., Huang, J., and Harbor, C. S. (2013). Structural plasticity of GABAergic axons is regulated by network activity and GABA A receptor activation. Front. Neural Circuits 7:113. doi: 10.3389/fncir.2013.00113.
175. Shen, K., and Bargmann, C. I. (2003). The immunoglobulin superfamily protein SYG-1 determines the location of specific synapses in C. elegans. Cell 112, 619-630. doi: 10.1016/S0092-8674(03)00113-2.
176. Shen, K., Fetter, R. D., and Bargmann, C. I. (2004). Synaptic specificity is generated by the synaptic guidepost protein SYG-2 and its receptor, SYG-1. Cell 116, 869-881. doi: 10.1016/S0092-8674(04)00251-X.
177. Shepherd, G. M., and Harris, K. M. (1998). Three-dimensional structure and composition of CA3->CA1 axons in rat hippocampal slices: implications for presynaptic connectivity and compartmentalization. J. Neurosci. 18, 8300-8310.
178. Siddiqui, T. J., and Craig, A. M. (2011). Synaptic organizing complexes. Curr. Opin. Neurobiol. 21, 132-143. doi: 10.1016/j.conb.2010.08.016.
179. Siddiqui, T. J., Tari, P. K., Connor, S. A., Zhang, P., Dobie, F. A., She, K., et al. (2013). An LRRTM4-HSPG complex mediates excitatory synapse development on dentate gyrus granule cells. Neuron 79, 680-695. doi: 10.1016/j.neuron.2013.06.029.
180. Staras, K. (2007). Share and share alike: trading of presynaptic elements between central synapses. Trends Neurosci. 30, 292-298. doi: 10.1016/j.tins.2007.04.005.
181. Staras, K., Branco, T., Burden, J. J., Pozo, K., Darcy, K., Marra, V., et al. (2010). A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron 66, 37-44. doi: 10.1016/j.neuron.2010.03.020.
182. Stellwagen, D., and Malenka, R. C. (2006). Synaptic scaling mediated by glial TNF-alpha. Nature 440, 1054-1059. doi: 10.1038/nature04671.
183. Stepanyants, A., Tamás, G., and Chklovskii, D. B. (2004). Class-specific features of neuronal wiring. Neuron 43, 251-259. doi: 10.1016/j.neuron.2004.06.013.
184. Su, J., Gorse, K., Ramirez, F., and Fox, M. A. (2010). Collagen XIX is expressed by interneurons and contributes to the formation of hippocampal synapses. J. Comp. Neurol. 518, 229-253. doi: 10.1002/cne.22228.
185. Südhof, T. C. (2008). Neuroligins and neurexins link synaptic function to cognitive disease. Nature 455, 903-911. doi: 10.1038/nature07456.
186. Sugita, S. (2001). A stoichiometric complex of neurexins and dystroglycan in brain. J. Cell Biol. 154, 435-446. doi: 10.1083/jcb.200105003.
187. Sumita, K., Sato, Y., Iida, J., Kawata, A., Hamano, M., Hirabayashi, S., et al. (2007). Synaptic scaffolding molecule (S-SCAM) membrane-associated guanylate kinase with inverted organization (MAGI)-2 is associated with cell adhesion molecules at inhibitory synapses in rat hippocampal neurons. J. Neurochem. 100, 154-166. doi: 10.1111/j.1471-4159.2006.04170.x.
188. Sun, Y., and Bamji, S. X. (2011). β-Pix modulates actin-mediated recruitment of synaptic vesicles to synapses. J. Neurosci. 31, 17123-17133. doi: 10.1523/JNEUROSCI.2359-11.2011.
189. Suzuki, K., Hayashi, Y., Nakahara, S., Kumazaki, H., Prox, J., Horiuchi, K., et al. (2012). Activity-dependent proteolytic cleavage of neuroligin-1. Neuron 76, 410-422. doi: 10.1016/j.neuron.2012.10.003.
190. Swanwick, C. C., Murthy, N. R., and Kapur, J. (2006). Activity-dependent scaling of GABAergic synapse strength is regulated by brain-derived neurotrophic factor. Mol. Cell. Neurosci. 31, 481-492. doi: 10.1016/j.mcn.2005.11.002.
191. Swiercz, J. M., Worzfeld, T., and Offermanns, S. (2008). ErbB-2 and met reciprocally regulate cellular signaling via plexin-B1. J. Biol. Chem. 283, 1893-1901. doi: 10.1074/jbc.M706822200.
192. Tabuchi, K., Biederer, T., Butz, S., and Sudhof, T. C. (2002). CASK participates in alternative tripartite complexes in which Mint 1 competes for binding with caskin 1, a novel CASK-binding protein. J. Neurosci. 22, 4264-4273.
193. Tai, C.-Y., Mysore, S. P., Chiu, C., and Schuman, E. M. (2007). Activity-regulated N-cadherin endocytosis. Neuron 54, 771-785. doi: 10.1016/j.neuron.2007.05.013.
194. Takahashi, H., and Craig, A. M. (2013). Protein tyrosine phosphatases PTPδ, PTPσ, and LAR: presynaptic hubs for synapse organization. Trends Neurosci. 36, 522-534. doi: 10.1016/j.tins.2013.06.002.
195. Takahashi, H., Katayama, K., Sohya, K., Miyamoto, H., Prasad, T., Matsumoto, Y., et al. (2012). Selective control of inhibitory synapse development by Slitrk3-PTPδ trans-synaptic interaction. Nat. Neurosci. 15, 389-398. doi: 10.1038/nn.3040.
196. Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., et al. (2006). Molecular anatomy of a trafficking organelle. Cell 127, 831-846. doi: 10.1016/j.cell.2006.10.030.
197. Taniguchi, H., Gollan, L., Scholl, F. G., Mahadomrongkul, V., Dobler, E., Limthong, N., et al. (2007). Silencing of neuroligin function by postsynaptic neurexins. J. Neurosci.27, 2815-2824. doi: 10.1523/JNEUROSCI.0032-07.2007.
198. Tasaka, G.-I., Negishi, M., and Oinuma, I. (2012). Semaphorin 4D/plexin-B1-mediated M-Ras GAP activity regulates actin-based dendrite remodeling through Lamellipodin.J. Neurosci. 32, 8293-8305. doi: 10.1523/JNEUROSCI.0799-12.2012.
199. Taylor, A. M., Berchtold, N. C., Perreau, V. M., Tu, C. H., Li Jeon, N., and Cotman, C. W. (2009). Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 29, 4697-4707. doi: 10.1523/JNEUROSCI.6130-08.2009.
200. Taylor, A. M., Wu, J., Tai, H.-C., and Schuman, E. M. (2013). Axonal translation of β-catenin regulates synaptic vesicle dynamics. J. Neurosci. 33, 5584-5589. doi: 10.1523/JNEUROSCI.2944-12.2013.
201. Terauchi, A., Johnson-Venkatesh, E. M., Toth, A. B., Javed, D., Sutton, M. A., and Umemori, H. (2010). Distinct FGFs promote differentiation of excitatory and inhibitory synapses. Nature 465, 783-787. doi: 10.1038/nature09041.
202. Thalhammer, A., and Cingolani, L. A. (2013). Cell adhesion and homeostatic synaptic plasticity. Neuropharmacology pii: S0028-3908(13)00111-1. doi: 10.1016/j.neuropharm.2013.03.015.
203. Ting, A. K., Chen, Y., Wen, L., Yin, D.-M., Shen, C., Tao, Y., et al. (2011). Neuregulin 1 promotes excitatory synapse development and function in GABAergic interneurons.J. Neurosci. 31, 15-25. doi: 10.1523/JNEUROSCI.2538-10.2011.
204. Turrigiano, G. (2011). Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu. Rev. Neurosci. 89-103. doi: 10.1146/annurev-neuro-060909-153238.
205. Turrigiano, G. G. (1999). Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci. 22, 221-227. doi: 10.1016/S0166-2236(98)01341-1.
206. Turrigiano, G. G. (2008). The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135, 422-435. doi: 10.1016/j.cell.2008.10.008.
207. Turrigiano, G. G., Leslie, K. R., Desai, N. S., Rutherford, L. C., and Nelson, S. B. (1998). Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892-896. doi: 10.1038/36103.
208. Tyagarajan, S. K., and Fritschy, J.-M. (2010). GABA(A) receptors, gephyrin and homeostatic synaptic plasticity. J. Physiol. 588, 101-106. doi: 10.1113/jphysiol.2009.178517.
209. Umemori, H., Linhoff, M. W., Ornitz, D. M., and Sanes, J. R. (2004). FGF22 and its close relatives are presynaptic organizing molecules in the mammalian brain. Cell 118, 257-270. doi: 10.1016/j.cell.2004.06.025.
210. vanVersendaal, D., Rajendran, R., Saiepour, M. H., Klooster, J., Smit-Rigter, L., Sommeijer, J.-P., et al. (2012). Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron 74, 374-383. doi: 10.1016/j.neuron.2012.03.015.
211. Varoqueaux, F., Aramuni, G., Rawson, R. L., Mohrmann, R., Missler, M., Gottmann, K., et al. (2006). Neuroligins determine synapse maturation and function. Neuron 51, 741-754. doi: 10.1016/j.neuron.2006.09.003.
212. Varoqueaux, F., Jamain, S., and Brose, N. (2004). Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 83, 449-456. doi: 10.1078/0171-9335-00410.
213. Verhage, M. (2000). Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287, 864-869. doi: 10.1126/science.287.5454.864.
214. Vicario-Abejón, C., Collin, C., Mckay, R. D. G., and Segal, M. (1998). Neurotrophins induce formation of functional excitatory and inhibitory synapses between cultured hippocampal neurons. J. Neurosci. 18, 7256-7271.
215. Vlachos, A., Reddy-Alla, S., Papadopoulos, T., Deller, T., and Betz, H. (2012). Homeostatic regulation of gephyrin scaffolds and synaptic strength at mature hippocampal GABAergic postsynapses. Cereb. Cortex 23, 2700-2711. doi: 10.1093/cercor/bhs260.
216. Vullhorst, D., Neddens, J., Karavanova, I., Tricoire, L., Petralia, R. S., McBain, C. J., et al. (2009). Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J. Neurosci. 29, 12255-12264. doi: 10.1523/JNEUROSCI.2454-09.2009.
217. Wen, L., Lu, Y.-S., Zhu, X.-H., Li, X.-M., Woo, R.-S., Chen, Y.-J., et al. (2010). Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc. Natl. Acad. Sci. U.S.A. 107, 1211-1216. doi: 10.1073/pnas.0910302107.
218. Wenner, P. (2011). Mechanisms of GABAergic homeostatic plasticity. Neural Plast.2011, 489470. doi: 10.1155/2011/489470.
219. Wentzel, C., Sommer, J. E., Nair, R., Stiefvater, A., Sibarita, J.-B., and Scheiffele, P. (2013). mSYD1A, a mammalian synapse-defective-1 protein, regulates synaptogenic signaling and vesicle docking. Neuron 78, 1012-1023. doi: 10.1016/j.neuron.2013.05.010.
220. Wierenga, C. J., Becker, N., and Bonhoeffer, T. (2008). GABAergic synapses are formed without the involvement of dendritic protrusions. Nat. Neurosci. 11, 1044-1052. doi: 10.1038/nn.2180.
221. Wierenga, C. J., Walsh, M. F., and Turrigiano, G. G. (2006). Temporal regulation of the expression locus of homeostatic plasticity. J. Neurophysiol. 96, 2127-33. doi: 10.1152/jn.00107.2006.
222. de Wit, J., O'Sullivan, M. L., Savas, J. N., Condomitti, G., Caccese, M. C., Vennekens, K. M., et al. (2013). Unbiased discovery of glypican as a receptor for LRRTM4 in regulating excitatory synapse development. Neuron 79, 696-711. doi: 10.1016/j.neuron.2013.06.049.
223. Wittenmayer, N., Körber, C., Liu, H., Kremer, T., Varoqueaux, F., Chapman, E. R., et al. (2009). Postsynaptic neuroligin1 regulates presynaptic maturation. Proc. Natl. Acad. Sci. U.S.A. 106, 13564-13569. doi: 10.1073/pnas.0905819106.
224. Wojtowicz, W. M., Wu, W., Andre, I., Qian, B., Baker, D., and Zipursky, S. L. (2007). A vast repertoire of Dscam binding specificities arises from modular interactions of variable Ig domains. Cell 130, 1134-1145. doi: 10.1016/j.cell.2007.08.026.
225. Woo, J., Kwon, S.-K., Nam, J., Choi, S., Takahashi, H., Krueger, D., et al. (2013). The adhesion protein IgSF9b is coupled to neuroligin 2 via S-SCAM to promote inhibitory synapse development. J. Cell Biol. 201, 929-944. doi: 10.1083/jcb.201209132.
226. Woo, R.-S., Li, X.-M., Tao, Y., Carpenter-Hyland, E., Huang, Y. Z., Weber, J., et al. (2007). Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54, 599-610. doi: 10.1016/j.neuron.2007.04.009.
227. Wu, X., Fu, Y., Knott, G., Lu, J., Di Cristo, G., and Huang, J. (2012). GABA signaling promotes synapse elimination and axon pruning in developing cortical inhibitory interneurons. J. Neurosci. 32, 331-343. doi: 10.1523/JNEUROSCI.3189-11.2012.
228. Wu, Y. E., Huo, L., Maeder, C. I., Feng, W., and Shen, K. (2013). The balance between capture and dissociation of presynaptic proteins controls the spatial distribution of synapses. Neuron 78, 994-1011. doi: 10.1016/j.neuron.2013.04.035.
229. Yamada, M. K., Nakanishi, K., Ohba, S., Nakamura, T., Ikegaya, Y., Nishiyama, N., et al. (2002). Brain-derived neurotrophic factor promotes the maturation of GABAergic mechanisms in cultured hippocampal neurons. J. Neurosci. 22, 7580-7585.
230. Yamada, T., Yang, Y., Huang, J., Coppola, G., Geschwind, D. H., and Bonni, A. (2013). Sumoylated MEF2A coordinately eliminates orphan presynaptic sites and promotes maturation of presynaptic boutons. J. Neurosci. 33, 4726-4740. doi: 10.1523/JNEUROSCI.4191-12.2013.
231. Yim, Y. S., Kwon, Y., Nam, J., In, H., Lee, K., Goo, D., et al. (2013). Slitrks control excitatory and inhibitory synapse formation with LAR receptor protein tyrosine phosphatases. Proc. Natl. Acad. Sci. U.S.A. 110, 4057-4062. doi: 10.1073/pnas.1209881110.
232. Yin, D.-M., Chen, Y.-J., Lu, Y.-S., Bean, J. C., Sathyamurthy, A., Shen, C., et al. (2013). Reversal of behavioral deficits and synaptic dysfunction in mice overexpressing neuregulin 1. Neuron 78, 644-657. doi: 10.1016/j.neuron.2013.03.028.
233. Yizhar, O., Fenno, L. E., Prigge, M., Schneider, F., Davidson, T. J., O'Shea, D. J., et al. (2011). Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171-178. doi: 10.1038/nature10360.
234. Yoshida, T., Shiroshima, T., Lee, S.-J., Yasumura, M., Uemura, T., Chen, X., et al. (2012). Interleukin-1 receptor accessory protein organizes neuronal synaptogenesis as a cell adhesion molecule. J. Neurosci. 32, 2588-2600. doi: 10.1523/JNEUROSCI.4637-11.2012.
235. Yoshida, T., Yasumura, M., Uemura, T., Lee, S.-J., Ra, M., Taguchi, R., et al. (2011). IL-1 receptor accessory protein-like 1 associated with mental retardation and autism mediates synapse formation by trans-synaptic interaction with protein tyrosine phosphatase δ. J. Neurosci. 31, 13485-13499. doi: 10.1523/JNEUROSCI.2136-11.2011.
236. Zander, J.-F., Münster-Wandowski, A., Brunk, I., Pahner, I., Gómez-Lira, G., Heinemann, U., et al. (2010). Synaptic and vesicular coexistence of VGLUT and VGAT in selected excitatory and inhibitory synapses. J. Neurosci. 30, 7634-7645. doi: 10.1523/JNEUROSCI.0141-10.2010.
237. Zhai, R. G., Vardinon-Friedman, H., Cases-Langhoff, C., Becker, B., Gundelfinger, E. D., Ziv, N. E., et al. (2001). Assembling the presynaptic active zone: a characterization of an active zone precursor vesicle. Neuron 29, 131-143. doi: 10.1016/S0896-6273(01)00185-4.
238. Zhang, Y., Luan, Z., Liu, A., and Hu, G. (2001). The scaffolding protein CASK mediates the interaction between rabphilin3a and beta-neurexins. FEBS Lett. 497, 99-102. doi: 10.1016/S0014-5793(01)02450-4.
239. Zhao, C., Dreosti, E., and Lagnado, L. (2011). Homeostatic synaptic plasticity through changes in presynaptic calcium influx. J. Neurosci. 31, 7492-7496. doi: 10.1523/JNEUROSCI.6636-10.2011.
240. Zhu, L., Bergmeier, W., Wu, J., Jiang, H., Stalker, T. J., Cieslak, M., et al. (2007). Regulated surface expression and shedding support a dual role for semaphorin 4D in platelet responses to vascular injury. Proc. Natl. Acad. Sci. U.S.A. 104, 1621-1626. doi: 10.1073/pnas.0606344104.
241. Zivraj, K. H., Tung, Y. C. L., Piper, M., Gumy, L., Fawcett, J. W., Yeo, G. S. H., and Holt, C. E. (2010). Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J. Neurosci. 30, 15464-15478. doi: 10.1523/JNEUROSCI.1800-10.2010.