Erratum to Integration and regulation of glomerular inhibition in the cerebellar granular layer circuit (Front. Cell. Neurosci., (2014) 8, (55), 10.3389/fncel.2014.00055;Integration and regulation of glomerular inhibition in the cerebellar granular layer circuit

Frontiers in Cellular Neuroscience

Volumn 8, Issue FEB, 2014, Pages

  Mapelli, Lisa ^a,b   Solinas, Sergio ^a,b   D'Angelo, Egidio ^a,b  

^a UNIVERSITY OF PAVIA   (Italy)

^b C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

Author keywords

Cerebellum; GABA receptors; Golgi cells; Granule cells; Synaptic inhibition

Indexed keywords

EID: 84926239198     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2016.00031     Document Type: Erratum

References (121)

1. Albus, J. (1971). The theory of cerebellar function. Math. Biosci. 10, 25-61. doi: 10.1016/0025-5564(71)90051-4
2. Arenz, A., Silver, R. A., Schaefer, A. T., and Margrie, T. W. (2008). The contribution of single synapses to sensory representation in vivo. Science 321, 977-980. doi: 10.1126/science.1158391
3. Armano, S., Rossi, P., Taglietti, V., and D'Angelo E. (2000). Long-term potentiation of intrinsic excitability at the mossy fiber-granule cell synapse of rat cerebellum. J. Neurosci. 20, 5208-5216.
4. Ben-Ari, Y., Tseeb, V., Raggozzino, D., Khazipov, R., and Gaiarsa, J. L. (1994). Gamma-Aminobutyric acid (GABA): a fast excitatory transmitter which may regulate the development of hippocampal neurones in early postnatal life. Prog. Brain Res. 102, 261-273. doi: 10.1016/S0079-6123(08)60545-2
5. Blackburn, T. (2010). GabaB receptor pharmacology-a tribute to norman bowery. Adv. Pharmacol. 58, xv-xvi, 1-464.
6. Brandalise, F., Mapelli, L., Gerber, U., and Rossi, P. (2012). Golgi cell-mediated activation of postsynaptic GABA(B) receptors induces disinhibition of the Golgi cell-granule cell synapse in rat cerebellum. PLoS ONE 7:e43417. doi: 10.1371/journal.pone.0043417
7. Brickley, S. G., Cull-Candy, S. G., and Farrant, M. (1996). Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J. Physiol. 497(Pt 3), 753-759.
8. Brickley, S. G., and Mody, I. (2012). Extrasynaptic GABA(A) receptors: their function in the CNS and implications for disease. Neuron 73, 23-34. doi: 10.1016/j.neuron.2011.12.012
9. Brickley, S. G., Revilla, V., Cull-Candy, S. G., Wisden, W., and Farrant, M. (2001). Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409, 88-92. doi: 10.1038/35051086
10. Bright, D. P., Renzi, M., Bartram, J., McGee, T. P., MacKenzie, G., Hosie, A. M., et al. (2011). Profound desensitization by ambient GABA limits activation of δ-containing GABAA receptors during spillover. J. Neurosci. 31, 753-763. doi: 10.1523/JNEUROSCI.2996-10.2011
11. Capogna, M., and Pearce, R. A. (2011). GA, ABA, slow: causes and consequences. Trends Neurosci. 34, 101-112. doi: 10.1016/j.tins.2010.10.005
12. Casado, M., Dieudonné, S., and Ascher, P. (2000). Presynaptic N-methyl-D-aspartate receptors at the parallel fiber-Purkinje cell synapse. Proc. Natl. Acad. Sci. U.S.A. 97, 11593-11597. doi: 10.1073/pnas.200354297
13. Cavelier, P., Hamann, M., Rossi, D., Mobbs, P., and Attwell, D. (2005). Tonic excitation and inhibition of neurons: ambient transmitter sources and computational consequences. Prog. Biophys. Mol. Biol. 87, 3-16. doi: 10.1016/j.pbiomolbio.2004.06.001
14. Cesana, E., Pietrajtis, K., Bidoret, C., Isope, P., D'Angelo, E., Dieudonné, S., et al. (2013). Granule cell ascending axon excitatory synapses onto Golgi cells implement a potent feedback circuit in the cerebellar granular layer. J. Neurosci. 33, 12430-12446. doi: 10.1523/JNEUROSCI.4897-11.2013
15. Chadderton, P., Margrie, T. W., and Häusser, M. (2004). Integration of quanta in cerebellar granule cells during sensory processing. Nature 428, 856-860. doi: 10.1038/nature02442
16. Chance, F. S., Abbott, L. F., and Reyes, A. D. (2002). Gain modulation from background synaptic input. Neuron 35, 773-782. doi: 10.1016/S0896-6273(02)00820-6
17. Cherubini, E., and Conti, F. (2001). Generating diversity at GABAergic synapses. Trends Neurosci. 24, 155-162. doi: 10.1016/S0166-2236(00)01724-0
18. Clements, J. D., and Silver, R. A. (2000). Unveiling synaptic plasticity: a new graphical and analytical approach. Trends Neurosci. 23, 105-113. doi: 10.1016/S0166-2236(99)01520-9
19. Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O., and Somogyi, P. (1995). Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75-78. doi: 10.1038/378075a0
20. Connelly, W. M., Errington, A. C., Di Giovanni, G., and Crunelli, V. (2013a). Metabotropic regulation of extrasynaptic GABA-A receptors. Front. Neural Cir. 7, 1-8. doi: 10.1523/JNEUROSCI.0317-11.2011
21. Connelly, W. M., Fyson, S. J., Errington, A. C., McCafferty, C. P., Cope, D. W., Di Giovanni, G., et al. (2013b). GABAB Receptors Regulate Extrasynaptic GABAA Receptors. J. Neurosci. 33, 3780-3785. doi: 10.1523/JNEUROSCI.4989-12.2013
22. Crowley, J. J., Fioravante, D., and Regehr, W. G. (2009). Dynamics of fast and slow inhibition from cerebellar golgi cells allow flexible control of synaptic integration. Neuron 63, 843-853. doi: 10.1016/j.neuron.2009.09.004
23. D'Angelo, E. (2008). The critical role of Golgi cells in regulating spatio-temporal integration and plasticity at the cerebellum input stage. Front. Neurosci. 2, 35-46. doi: 10.3389/neuro.01.008.2008
24. D'Angelo, E., De Filippi, G., Rossi, P., and Taglietti, V. (1995). Synaptic excitation of individual rat cerebellar granule cells in situ: evidence for the role of NMDA receptors. J. Physiol. 484(Pt 2), 397-413.
25. D'Angelo, E., and De Zeeuw, C. I. (2009). Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci. 32, 30-40. doi: 10.1016/j.tins.2008.09.007
26. D'Angelo, E., Solinas, S., Mapelli, J., Gandolfi, D., Mapelli, L., and Prestori, F. (2013). The cerebellar Golgi cell and spatiotemporal organization of granular layer activity. Front. Neural Cir. 7:93. doi: 10.3389/fncir.2013.00093
27. Diaz, M. R., Wadleigh, A., Hughes, B. A., Woodward, J. J., and Valenzuela, C. F. (2011). Bestrophin1 channels are insensitive to ethanol and do not mediate tonic GABAergic currents in cerebellar granule cells. Front. Neurosci. 5:148. doi: 10.3389/fnins.2011.00148
28. Diaz, M. R., Wadleigh, A., Kumar, S., De Schutter, E., and Valenzuela, C. F. (2013). Na+/K+-ATPase inhibition partially mimics the ethanol-induced increase of the Golgi cell-dependent component of the tonic GABAergic current in rat cerebellar granule cells. PLoS ONE 8:e55673. doi: 10.1371/journal.pone.0055673
29. Dieudonne, S. (1998). Submillisecond kinetics and low efficacy of parallel fibre-Golgi cell synaptic currents in the rat cerebellum. J. Physiol. 510(Pt 3), 845-866. doi: 10.1111/j.1469-7793.1998.845bj.x
30. Dieudonné, S., and Dumoulin, A. (2000). Serotonin-driven long-range inhibitory connections in the cerebellar cortex. J. Neurosci. 20, 1837-1848. doi: 10.3389/fncir.2013.00093
31. Duguid, I., Branco, T., London, M., Chadderton, P., and Häusser, M. (2012). Tonic inhibition enhances fidelity of sensory information transmission in the cerebellar cortex. J. Neurosci. 32, 11132-11143. doi: 10.1523/JNEUROSCI.0460-12.2012
32. Eccles, J. C. (1967). Circuits in the cerebellar control of movement. Proc. Natl. Acad. Sci. U.S.A. 58, 336-343. doi: 10.1073/pnas.58.1.336
33. Eccles, J., Llinas, R., and Sasaki, K. (1964). Golgi cell inhibition in the cerebellar cortex. Nature 204, 1265-1266. doi: 10.1038/2041265a0
34. Edgley, S. A., and Lidierth, M. (1987). The discharges of cerebellar Golgi cells during locomotion in the cat. J. Physiol. 392, 315-332.
35. Edwards, F. A., Konnerth, A., and Sakmann, B. (1990). Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. J. Physiol. 430, 213-249.
36. Eyre, M. D., Renzi, M., Farrant, M., and Nusser, Z. (2012). Setting the time course of inhibitory synaptic currents by mixing multiple GABA(A) receptor α subunit isoforms. J. Neurosci. 32, 5853-5867. doi: 10.1523/JNEUROSCI.6495-11.2012
37. Farrant, M., and Nusser, Z. (2005). Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci. 6, 215-229. doi: 10.1038/nrn1625
38. Forti, L., Cesana, E., Mapelli, J., and D'Angelo, E. (2006). Ionic mechanisms of autorhythmic firing in rat cerebellar Golgi cells. J Physiol 574, 711-729. doi: 10.1113/jphysiol.2006.110858
39. Freund, T. F. (2003). Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci. 26, 489-495. doi: 10.1016/S0166-2236(03)00227-3
40. Gabbiani, F., Midtgaard, J., and Knöpfel, T. (1994). Synaptic integration in a model of cerebellar granule cells. J. Neurophysiol. 72, 999-1009.
41. Galarreta, M., and Hestrin, S. (2001). Electrical synapses between GABA-releasing interneurons. Nat. Rev. Neurosci. 2, 425-433. doi: 10.1038/35077566
42. Galliano, E., Mazzarello, P., and D'Angelo, E. (2010). Discovery and rediscoveries of Golgi cells. J. Physiol. 588, 3639-3655. doi: 10.1113/jphysiol.2010.189605
43. Galvez, T., Urwyler, S., Prézeau, L., Mosbacher, J., Joly, C., Malitschek, B., et al. (2000). Ca(2+) requirement for high-affinity gamma-aminobutyric acid (GABA) binding at GABA(B) receptors: involvement of serine 269 of the GABA(B)R1 subunit. Mol. Pharmacol. 57, 419-426.
44. Gandolfi, D., Lombardo, P., Mapelli, J., Solinas, S., and D'Angelo, E. (2013). Theta-frequency resonance at the cerebellum input stage improves spike timing on the millisecond time-scale. Front. Neural Cir. 7:64.
45. Garrido, J. A., Luque, N. R., D'Angelo, E., and Ros, E. (2013a). Distributed cerebellar plasticity implements adaptable gain control in a manipulation task: a closed-loop robotic simulation. Front. Neural Cir. 7:159.
46. Garrido, J. A., Ros, E., and D'Angelo, E. (2013b). Spike timing regulation on the millisecond scale by distributed synaptic plasticity at the cerebellum input stage: a simulation study. Front. Comput. Neurosci. 7:64. doi: 10.3389/fncom.2013.00064
47. Glykys, J., and Mody, I. (2007). Activation of GABAA receptors: views from outside the synaptic cleft. Neuron 56, 763-770. doi: 10.1016/j.neuron.2007.11.002
48. Hamann, M., Rossi, D. J., and Attwell, D. (2002). Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33, 625-633. doi: 10.1016/S0896-6273(02)00593-7
49. Hámori, J., and Somogyi, J. (1983). Differentiation of cerebellar mossy fiber synapses in the rat: a quantitative electron microscope study. J. Comp. Neurol. 220, 365-377. doi: 10.1002/cne.902200402
50. Holt, G. R., and Koch, C. (1997). Shunting inhibition does not have a divisive effect on firing rates. Neural Comput. 9, 1001-1013. doi: 10.1162/neco.1997.9.5.1001
51. Holtzman, T., Rajapaksa, T., Mostofi, A., and Edgley, S. A. (2006). Different responses of rat cerebellar Purkinje cells and Golgi cells evoked by widespread convergent sensory inputs. J. Physiol. 574, 491-507. doi: 10.1113/jphysiol.2006.108282
52. Hull, C. A., Chu, Y., Thanawala, M., and Regehr, W. G. (2013). Hyperpolarization induces a long-term increase in the spontaneous firing rate of cerebellar Golgi cells. J. Neurosci. 33, 5895-5902. doi: 10.1523/JNEUROSCI.4052-12.2013
53. Hull, C., and Regehr, W. G. (2012). Identification of an inhibitory circuit that regulates cerebellar Golgi cell activity. Neuron 73, 149-158. doi: 10.1016/j.neuron.2011.10.030
54. Jaarsma, D., Ruigrok, T. J., Caffé, R., Cozzari, C., Levey, A. I., Mugnaini, E., et al. (1997). Cholinergic innervation and receptors in the cerebellum. Prog. Brain Res. 114, 67-96. doi: 10.1016/S0079-6123(08)63359-2
55. Jakab, R. L., and Hámori, J. (1988). Quantitative morphology and synaptology of cerebellar glomeruli in the rat. Anat. Embryol. (Berl.) 179, 81-88. doi: 10.1007/BF00305102
56. Jensen, K., Chiu, C. S., Sokolova, I., Lester, H. A., and Mody, I. (2003). GABA transporter-1 (GAT1)-deficient mice: differential tonic activation of GABAA versus GABAB receptors in the hippocampus. J. Neurophysiol. 90, 2690-2701. doi: 10.1152/jn.00240.2003
57. Jonas, P., Bischofberger, J., Fricker, D., and Miles, R. (2004). Interneuron diversity series: fast in, fast out-temporal and spatial signal processing in hippocampal interneurons. Trends Neurosci. 27, 30-40. doi: 10.1016/j.tins.2003.10.010
58. Jones, A., Korpi, E. R., McKernan, R. M., Pelz, R., Nusser, Z., Mäkelä, R., et al. (1997). Ligand-gated ion channel subunit partnerships: GABAA receptor alpha6 subunit gene inactivation inhibits delta subunit expression. J. Neurosci. 17, 1350-1362.
59. Kaneda, M., Farrant, M., and Cull-Candy, S. G. (1995). Whole-cell and single-channel currents activated by GABA and glycine in granule cells of the rat cerebellum. J. Physiol. 485(Pt 2), 419-435.
60. Kanichay, R. T., and Silver, R. A. (2008). Synaptic and cellular properties of the feedforward inhibitory circuit within the input layer of the cerebellar cortex. J. Neurosci. 28, 8955-8967. doi: 10.1523/JNEUROSCI.5469-07.2008
61. Kase, M., Miller, D. C., and Noda, H. (1980). Discharges of Purkinje cells and mossy fibres in the cerebellar vermis of the monkey during saccadic eye movements and fixation. J. Physiol. 300, 539-555.
62. Katz, B., and Miledi, R. (1965). The effect of calcium on acetylcholine release from motor nerve terminals. Proc. R Soc. Lond B Biol. Sci. 161, 496-503. doi: 10.1098/rspb.1965.0017
63. Kozlov, A. S., Angulo, M. C., Audinat, E., and Charpak, S. (2006). Target cell-specific modulation of neuronal activity by astrocytes. Proc. Natl. Acad. Sci. U.S.A. 103, 10058-10063. doi: 10.1073/pnas.0603741103
64. Kulik, A., Nakadate, K., Nyíri, G., Notomi, T., Malitschek, B., Bettler, B., et al. (2002). Distinct localization of GABA(B) receptors relative to synaptic sites in the rat cerebellum and ventrobasal thalamus. Eur. J. Neurosci. 15, 291-307. doi: 10.1046/j.0953-816x.2001.01855.x
65. Lee, S., Yoon, B. E., Berglund, K., Oh, S. J., Park, H., Shin, H. S., et al. (2010). Channel-mediated tonic GABA release from glia. Science 330, 790-796. doi: 10.1126/science.1184334
66. Luscher, B., Fuchs, T., and Kilpatrick, C. L. (2011). GABAA receptor trafficking-mediated plasticity of inhibitory synapses. Neuron 70, 385-409. doi: 10.1016/j.neuron.2011.03.024
67. Maex, R., and De Schutter, E. (1998). Synchronization of golgi and granule cell firing in a detailed network model of the cerebellar granule cell layer. J. Neurophysiol. 80, 2521-2537.
68. Maffei, A., Prestori, F., Shibuki, K., Rossi, P., Taglietti, V., and D'Angelo, E. (2003). NO enhances presynaptic currents during cerebellar mossy fiber-granule cell LTP. J. Neurophysiol. 90, 2478-2483. doi: 10.1152/jn.00399.2003
69. Mapelli, J., and D'Angelo, E. (2007). The spatial organization of long-term synaptic plasticity at the input stage of cerebellum. J. Neurosci. 27, 1285-1296. doi: 10.1523/JNEUROSCI.4873-06.2007
70. Mapelli, J., Gandolfi, D., and D'Angelo, E. (2010a). Combinatorial responses controlled by synaptic inhibition in the cerebellum granular layer. J. Neurophysiol. 103, 250-261. doi: 10.1152/jn.00642.2009
71. Mapelli, J., Gandolfi, D., and D'Angelo, E. (2010b). High-pass filtering and dynamic gain regulation enhance vertical bursts transmission along the mossy fiber pathway of cerebellum. Front. Cell. Neurosci. 4:14. doi: 10.3389/fncel.2010.00014
72. Mapelli, L., Rossi, P., Nieus, T., and D'Angelo, E. (2009). Tonic activation of GABAB receptors reduces release probability at inhibitory connections in the cerebellar glomerulus. J. Neurophysiol. 101, 3089-3099. doi: 10.1152/jn.91190.2008
73. Marr, D. (1969). A theory of cerebellar cortex. J. Physiol. 202, 437-470.
74. Mitchell, S. J., and Silver, R. A. (2000a). GABA spillover from single inhibitory axons suppresses low-frequency excitatory transmission at the cerebellar glomerulus. J. Neurosci. 20, 8651-8658.
75. Mitchell, S. J., and Silver, R. A. (2000b). Glutamate spillover suppresses inhibition by activating presynaptic mGluRs. Nature 404, 498-502. doi: 10.1038/35006649
76. Mitchell, S. J., and Silver, R. A. (2003). Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38, 433-445. doi: 10.1016/S0896-6273(03)00200-9
77. Mohr, C., Kolotushkina, O., Kaplan, J. S., Welsh, J., Daunais, J. B., Grant, K. A., et al. (2013). Primate cerebellar granule cells exhibit a tonic GABAAR conductance that is not affected by alcohol: a possible cellular substrate of the low level of response phenotype. Front. Neural Cir. 7:189. doi: 10.3389/fncir.2013.00189
78. Nieus, T., Sola, E., Mapelli, J., Saftenku, E., Rossi, P., and D'Angelo, E. (2006). LTP regulates burst initiation and frequency at mossy fiber-granule cell synapses of rat cerebellum: experimental observations and theoretical predictions. J. Neurophysiol. 95, 686-699. doi: 10.1152/jn.00696.2005
79. Nusser, Z., Ahmad, Z., Tretter, V., Fuchs, K., Wisden, W., Sieghart, W., et al. (1999). Alterations in the expression of GABAA receptor subunits in cerebellar granule cells after the disruption of the alpha6 subunit gene. Eur. J. Neurosci. 11, 1685-1697. doi: 10.1046/j.1460-9568.1999.00581.x
80. Nusser, Z., Roberts, J. D., Baude, A., Richards, J. G., and Somogyi, P. (1995). Relative densities of synaptic and extrasynaptic GABAA receptors on cerebellar granule cells as determined by a quantitative immunogold method. J. Neurosci. 15, 2948-2960.
81. Nusser, Z., Sieghart, W., and Somogyi, P. (1998). Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J. Neurosci. 18, 1693-1703.
82. Olsen, R. W., and Sieghart, W. (2008). International Union of Pharmacology. LXX. Subtypes of gamma-aminobutyric acid(A) receptors: classification on the basis of subunit composition, pharmacology, and function. Update. Pharmacol. Rev. 60, 243-260. doi: 10.1124/pr.108.00505
83. 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
84. Orser, B. A. (2006). Extrasynaptic GABAA receptors are critical targets for sedative-hypnotic drugs. J. Clin. Sleep Med. 2, S12-S18.
85. Otis, T. S., Staley, K. J., and Mody, I. (1991). Perpetual inhibitory activity in mammalian brain slices generated by spontaneous GABA release. Brain Res. 545, 142-150. doi: 10.1016/0006-8993(91)91280-E
86. Palay, S. L., and Chan-Palay, V. (1974). Cerebellar Cortex: Cytology and Organization. New York, NY: Springer-Verlag. doi: 10.1007/978-3-642-65581-4
87. Palkovits, M., Magyar, P., and Szentágothai, J. (1971). Quantitative histological analysis of the cerebellar cortex in the cat. II. Cell numbers and densities in the granular layer. Brain Res. 32, 15-30. doi: 10.1016/0006-8993(71)90152-1
88. Payne, H. L., Ives, J. H., Sieghart, W., and Thompson, C. L. (2008). AMPA and kainate receptors mediate mutually exclusive effects on GABA(A) receptor expression in cultured mouse cerebellar granule neurones. J. Neurochem. 104, 173-186. doi: 10.1111/j.1471-4159.2007.04989.x
89. Prestori, F., Bonardi, C., Mapelli, L., Lombardo, P., Goselink, R., De Stefano, M. E., et al. (2013). Gating of long-term potentiation by nicotinic acetylcholine receptors at the cerebellum input stage. PLoS ONE 8:e64828. doi: 10.1371/journal.pone.0064828
90. Puia, G., Costa, E., and Vicini, S. (1994). Functional diversity of GABA-activated Cl-currents in Purkinje versus granule neurons in rat cerebellar slices. Neuron 12, 117-126. doi: 10.1016/0896-6273(94)90157-0
91. Rancz, E. A., Ishikawa, T., Duguid, I., Chadderton, P., Mahon, S., and Häusser, M. (2007). High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450, 1245-1248. doi: 10.1038/nature05995
92. Richerson, G. B. (2004). Looking for GABA in all the wrong places: the relevance of extrasynaptic GABA(A) receptors to epilepsy. Epilepsy Curr. 4, 239-242. doi: 10.1111/j.1535-7597.2004.46008.x
93. Robberechts, Q., Wijnants, M., Giugliano, M., and De Schutter, E. (2010). Long-term depression at parallel fiber to Golgi cell synapses. J. Neurophysiol. 104, 3413-3423. doi: 10.1152/jn.00030.2010
94. Rossi, D. J., and Hamann, M. (1998). Spillover-mediated transmission at inhibitory synapses promoted by high affinity alpha6 subunit GABA(A) receptors and glomerular geometry. Neuron 20, 783-795. doi: 10.1016/S0896-6273(00)81016-8
95. Rossi, D. J., Hamann, M., and Attwell, D. (2003). Multiple modes of GABAergic inhibition of rat cerebellar granule cells. J. Physiol. 548, 97-110. doi: 10.1113/jphysiol.2002.036459
96. Rossi, P., Mapelli, L., Roggeri, L., Gall, D., de Kerchove d'Exaerde, A., Schiffmann, S. N., et al. (2006). Inhibition of constitutive inward rectifier currents in cerebellar granule cells by pharmacological and synaptic activation of GABA receptors. Eur. J. Neurosci. 24, 419-432. doi: 10.1111/j.1460-9568.2006.04914.x
97. Santhakumar, V., Hanchar, H. J., Wallner, M., Olsen, R. W., and Otis, T. S. (2006). Contributions of the GABAA receptor alpha6 subunit to phasic and tonic inhibition revealed by a naturally occurring polymorphism in the alpha6 gene. J. Neurosci. 26, 3357-3364. doi: 10.1523/JNEUROSCI.4799-05.2006
98. Sassoè-Pognetto, M., Panzanelli, P., Sieghart, W., and Fritschy, J. M. (2000). Colocalization of multiple GABA(A) receptor subtypes with gephyrin at postsynaptic sites. J. Comp. Neurol. 420, 481-498. doi: 10.1002/(SICI)1096-9861(20000515)420:4<481::AID-CNE6>3.0.CO;2-5
99. Saxena, N. C., and Macdonald, R. L. (1994). Assembly of GABAA receptor subunits: role of the delta subunit. J. Neurosci. 14, 7077-7086.
100. Saxena, N. C., and Macdonald, R. L. (1996). Properties of putative cerebellar gamma-aminobutyric acid A receptor isoforms. Mol. Pharmacol. 49, 567-579.
101. Schweighofer, N., Doya, K., and Lay, F. (2001). Unsupervised learning of granule cell sparse codes enhances cerebellar adaptive control. Neuroscience 103, 35-50. doi: 10.1016/S0306-4522(00)00548-0
102. Semyanov, A., Walker, M. C., and Kullmann, D. M. (2003). GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat. Neurosci. 6, 484-490. doi: 10.1038/nn1043
103. Semyanov, A., Walker, M. C., Kullmann, D. M., and Silver, R. A. (2004). Tonically active GABA A receptors: modulating gain and maintaining the tone. Trends Neurosci. 27, 262-269. doi: 10.1016/j.tins.2004.03.005
104. Singer, W., and Gray, C. M. (1995). Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555-586. doi: 10.1146/annurev.ne.18.030195.003011
105. Sola, E., Prestori, F., Rossi, P., Taglietti, V., and D'Angelo, E. (2004). Increased neurotransmitter release during long-term potentiation at mossy fibre-granule cell synapses in rat cerebellum. J. Physiol. 557, 843-861. doi: 10.1113/jphysiol.2003.060285
106. Solinas, S., Forti, L., Cesana, E., Mapelli, J., De Schutter, E., and D'Angelo, E. (2007a). Computational reconstruction of pacemaking and intrinsic electroresponsiveness in cerebellar Golgi cells. Front. Cell. Neurosci. 1:2. doi: 10.3389/neuro.03.002.2007
107. Solinas, S., Forti, L., Cesana, E., Mapelli, J., De Schutter, E., and D'Angelo, E. (2007b). Fast-reset of pacemaking and theta-frequency resonance patterns in cerebellar golgi cells: simulations of their impact in vivo. Front. Cell. Neurosci. 1:4. doi: 10.3389/neuro.03.004.2007
108. Solinas, S., Nieus, T., and D'Angelo, E. (2010). A realistic large-scale model of the cerebellum granular layer predicts circuit spatio-temporal filtering properties. Front. Cell. Neurosci. 4:12. doi: 10.3389/fncel.2010.00012
109. Stell, B. M., Brickley, S. G., Tang, C. Y., Farrant, M., and Mody, I. (2003). Neuroactive steroids reduce neuronal excitability by selectively enhancing tonic inhibition mediated by delta subunit-containing GABAA receptors. Proc. Natl. Acad. Sci. U.S.A. 100, 14439-14444. doi: 10.1073/pnas.2435457100
110. Uusi-Oukari, M., Kontturi, L. S., Coffey, E. T., and Kallinen, S. A. (2010). AMPAR signaling mediating GABA(A)R delta subunit up-regulation in cultured mouse cerebellar granule cells. Neurochem. Int. 57, 136-142. doi: 10.1016/j.neuint.2010.05.005
111. Valeyev, A. Y., Cruciani, R. A., Lange, G. D., Smallwood, V. S., and Barker, J. L. (1993). Cl-channels are randomly activated by continuous GABA secretion in cultured embryonic rat hippocampal neurons. Neurosci. Lett. 155, 199-203. doi: 10.1016/0304-3940(93)90707-R
112. Vervaeke, K., Lorincz, A., Gleeson, P., Farinella, M., Nusser, Z., and Silver, R. A. (2010). Rapid desynchronization of an electrically coupled interneuron network with sparse excitatory synaptic input. Neuron 67, 435-451. doi: 10.1016/j.neuron.2010.06.028
113. Vithlani, M., Terunuma, M., and Moss, S. J. (2011). The dynamic modulation of GABA(A) receptor trafficking and its role in regulating the plasticity of inhibitory synapses. Physiol. Rev. 91, 1009-1022. doi: 10.1152/physrev.00015.2010
114. Vizi, E. S., and Mike, A. (2006). Nonsynaptic receptors for GABA and glutamate. Curr. Top. Med. Chem. 6, 941-948. doi: 10.2174/156802606777323782
115. Vos, B. P., Volny-Luraghi, A., and De Schutter, E. (1999). Cerebellar Golgi cells in the rat: receptive fields and timing of responses to facial stimulation. Eur. J. Neurosci. 11, 2621-2634. doi: 10.1046/j.1460-9568.1999.00678.x
116. Wall, M. J. (2002). Furosemide reveals heterogeneous GABA(A) receptor expression at adult rat Golgi cell to granule cell synapses. Neuropharmacology 43, 737-749. doi: 10.1016/S0028-3908(02)00085-0
117. Wall, M. J. (2003). Endogenous nitric oxide modulates GABAergic transmission to granule cells in adult rat cerebellum. Eur. J. Neurosci. 18, 869-878. doi: 10.1046/j.1460-9568.2003.02822.x
118. Wall, M. J., and Usowicz, M. M. (1997). Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur. J. Neurosci. 9, 533-548. doi: 10.1111/j.1460-9568.1997.tb01630.x
119. Watanabe, D., and Nakanishi, S. (2003). mGluR2 postsynaptically senses granule cell inputs at Golgi cell synapses. Neuron 39, 821-829. doi: 10.1016/S0896-6273(03)00530-0
120. Whiting, P. J. (2003). GABA-A receptor subtypes in the brain: a paradigm for CNS drug discovery? Drug Discov. Today 8, 445-450. doi: 10.1016/S1359-6446(03)02703-X
121. Zheleznova, N. N., Sedelnikova, A., and Weiss, D. S. (2009). Function and modulation of delta-containing GABA(A) receptors. Psychoneuroendocrinology 34(Suppl. 1), S67-S73. doi: 10.1016/j.psyneuen.2009.08.010