Rebound discharge in deep cerebellar nuclear neurons in vitro

Cerebellum

Volumn 9, Issue 3, 2010, Pages 352-374

  Tadayonnejad, Reza ^a   Anderson, Dustin ^a   Molineux, Michael L ^a   Mehaffey, W Hamish ^a   Jayasuriya, Kusala ^a   Turner, Ray W ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Afterhyperpolarization; DCN; Purkinje cell; Rebound bursts; T type channel

Indexed keywords

CALCIUM; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL T TYPE;

AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL TISSUE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CEREBELLUM NUCLEUS; CONTROLLED STUDY; EVOKED RESPONSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; RAT; REVIEW; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM CHANNELS, T-TYPE; CEREBELLAR NUCLEI; MEMBRANE POTENTIALS; NEURONS; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 78049269883     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-010-0168-7     Document Type: Review

References (124)

1. U Czubayko F Sultan P Thier C Schwarz 2001 Two types of neurons in the rat cerebellar nuclei as distinguished by membrane potentials and intracellular fillings J Neurophysiol 85 5 2017 2029 1:STN:280:DC%2BD3M3lsVyhuw%3D%3D 11353018
2. CD Aizenman DJ Linden 1999 Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum J Neurophysiol 82 4 1697 1709 1:CAS:528:DyaK1MXmvVyltr8%3D 10515960
3. M Uusisaari K Obata T Knopfel 2007 Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei J Neurophysiol 97 1 901 911 1:CAS:528:DC%2BD2sXhvVOmtbk%3D 17093116
4. H Jahnsen 1986 Extracellular activation and membrane conductances of neurones in the guinea-pig deep cerebellar nuclei in vitro J Physiol 372 149 168 1:STN:280:DyaL283ltlyqsw%3D%3D 2425083 (Pubitemid 16048147)
5. IM Raman AE Gustafson D Padgett 2000 Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei J Neurosci 20 24 9004 9016 1:CAS:528:DC%2BD3MXis1Srsg%3D%3D 11124976
6. R Gardette M Debono JL Dupont F Crepel 1985 Electrophysiological studies on the postnatal development of intracerebellar nuclei neurons in rat cerebellar slices maintained in vitro. II. Membrane conductances Brain Res 352 1 97 106 1:STN:280:DyaL2M3islCrtA%3D%3D 2408714 (Pubitemid 15008520)
7. ML Molineux JE McRory BE McKay J Hamid WH Mehaffey R Rehak, et al. 2006 Specific T-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons Proc Natl Acad Sci USA 103 14 5555 5560 1:CAS:528:DC%2BD28XjslejsL4%3D 16567615
8. ML Molineux WH Mehaffey R Tadayonnejad D Anderson AF Tennent RW Turner 2008 Ionic factors governing rebound burst phenotype in rat deep cerebellar neurons J Neurophysiol 100 5 2684 2701 18768644
9. R Llinas M Muhlethaler 1988 Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation J Physiol 404 241 258 1:STN:280:DyaL1MzhtFWhug%3D%3D 2855348
10. N Zheng IM Raman 2009 Ca currents activated by spontaneous firing and synaptic disinhibition in neurons of the cerebellar nuclei J Neurosci 29 31 9826 9838 1:CAS:528:DC%2BD1MXpvFOmurs%3D 19657035
11. ML Molineux FR Fernandez WH Mehaffey RW Turner 2005 A-type and T-type currents interact to produce a novel spike latency-voltage relationship in cerebellar stellate cells J Neurosci 25 47 10863 10873 1:CAS:528: DC%2BD2MXht1yks77L 16306399
12. CD Aizenman EJ Huang DJ Linden 2003 Morphological correlates of intrinsic electrical excitability in neurons of the deep cerebellar nuclei J Neurophysiol 89 1738 1747 12686564
13. CD Aizenman PB Manis DJ Linden 1998 Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse Neuron 21 4 827 835 1:CAS:528:DyaK1cXnt1Sgu70%3D 9808468
14. R Gardette M Debono JL Dupont F Crepel 1985 Electrophysiological studies on the postnatal development of intracerebellar nuclei neurons in rat cerebellar slices maintained in vitro. I. Postsynaptic potentials Brain Res 351 1 47 55 1:STN:280:DyaL2M3gtV2ntw%3D%3D 2986789 (Pubitemid 15075735)
15. W Zhang JH Shin DJ Linden 2004 Persistent changes in the intrinsic excitability of rat deep cerebellar nuclear neurons induced by EPSPs or IPSP bursts J Physiol (Lond) 561.3 703 19
16. R Tadayonnejad WH Mehaffey D Anderson RW Turner 2009 Reliability of triggering postinhibitory rebound bursts in deep cerebellar neurons Channels 3 3 1 7
17. K Alvina JT Walter A Kohn G Ellis-Davies K Khodakhah 2008 Questioning the role of rebound firing in the cerebellum Nat Neurosci 11 11 1256 1258 1:CAS:528:DC%2BD1cXht12ltrrI 18820695
18. DM Armstrong B Cogdell RJ Harvey 1973 Response of interpositus neurones to nerve stimulation in chloralose anesthetized cats Brain Res 55 2 461 466 1:STN:280:DyaE3s3gsF2isw%3D%3D 4714015
19. RA McCrea GA Bishop ST Kitai 1977 Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior. II. Mossy fiber system Brain Res 122 2 215 228 1:STN:280: DyaE2s7htlCmtQ%3D%3D 837229
20. ST Kitai RA McCrea RJ Preston GA Bishop 1977 Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior. I. Climbing fiber system Brain Res 122 2 197 214 1:STN:280:DyaE2s7htlCmtA%3D%3D 837228
21. M Ito M Yoshida K Obata N Kawai M Udo 1970 Inhibitory control of intracerebellar nuclei by the purkinje cell axons Exp Brain Res 10 1 64 80 1:STN:280:DyaE3c%2FptFahsg%3D%3D 5411975
22. NC Rowland D Jaeger 2008 Responses to tactile stimulation in deep cerebellar nucleus neurons result from recurrent activation in multiple pathways J Neurophysiol 99 2 704 717 18077662
23. TJ Ruigrok 1997 Cerebellar nuclei: the olivary connection Prog Brain Res 114 167 192 1:STN:280:DyaK2szjs1erug%3D%3D 9193144
24. A Gruart AM Pastor JA Armengol JM Delgado-Garcia 1997 Involvement of cerebellar cortex and nuclei in the genesis and control of unconditioned and conditioned eyelid motor responses Prog Brain Res 114 511 528 1:STN:280:DyaK2szjs1CjtQ%3D%3D 9193163
25. FP Chen C Evinger 2006 Cerebellar modulation of trigeminal reflex blinks: interpositus neurons J Neurosci 26 41 10569 10576 1:CAS:528:DC%2BD28XhtFegur3I 17035543
26. NC Rowland D Jaeger 2005 Coding of tactile response properties in the rat deep cerebellar nuclei J Neurophysiol 94 2 1236 1251 16061491
27. K Ohtsuka H Noda 1991 Saccadic burst neurons in the oculomotor region of the fastigial nucleus of macaque monkeys J Neurophysiol 65 6 1422 1434 1:STN:280:DyaK3MzktFGksg%3D%3D 1875251
28. DM Armstrong B Cogdell R Harvey 1975 Effects of afferent volleys from the limbs on the discharge patterns of interpositus neurones in cats anaesthetized with alpha-chloralose J Physiol 248 2 489 517 1:STN:280:DyaE2M3htlOksw%3D%3D 1151794
29. WA MacKay 1988 Unit activity in the cerebellar nuclei related to arm reaching movements Brain Res 442 2 240 254 1:STN:280:DyaL1c3it1Onug%3D%3D 3370446
30. AB Schwartz TJ Ebner JR Bloedel 1987 Responses of interposed and dentate neurons to perturbations of the locomotor cycle Exp Brain Res 67 2 323 338 1:STN:280:DyaL2szgsVKqtg%3D%3D 3622692
31. JM Delgado-Garcia A Gruart 2005 Firing activities of identified posterior interpositus nucleus neurons during associative learning in behaving cats Brain Res Brain Res Rev 49 2 367 376 16111563
32. JR Pugh IM Raman 2006 Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current Neuron 51 1 113 123 1:CAS:528:DC%2BD28XnsVWgs7o%3D 16815336
33. J Hamid JB Peloquin A Monteil GW Zamponi 2006 Determinants of the differential gating properties of Cav3.1 and Cav3.3 T-type channels: a role of domain IV? Neuroscience 143 3 717 728 1:CAS:528:DC%2BD28Xht1agt7%2FF 16996222
34. Chan-Palay V (1977) Cerebellar dentate nucleus: organization, cytology and transmitters. Springer, Berlin
35. F Sultan U Czubayko P Thier 2003 Morphological classification of the rat lateral cerebellar nuclear neurons by principal component analysis J Comp Neurol 455 2 139 155 12454981
36. DM Armstrong JA Rawson 1979 Activity patterns of cerebellar cortical neurones and climbing fibre afferents in the awake cat J Physiol 289 425 448 1:STN:280:DyaE1M3hvVGhsw%3D%3D 458677
37. FW Cody RB Moore HC Richardson 1981 Patterns of activity evoked in cerebellar interpositus nuclear neurones by natural somatosensory stimuli in awake cats J Physiol 317 1 20 1:STN:280:DyaL38%2FnslOnuw%3D%3D 7310728
38. MS LeDoux DC Hurst JF Lorden 1998 Single-unit activity of cerebellar nuclear cells in the awake genetically dystonic rat Neuroscience 86 2 533 545 1:CAS:528:DyaK1cXktlGgtbs%3D 9881867
39. V Gauck D Jaeger 2000 The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition J Neurosci 20 8 3006 3016 1:CAS:528:DC%2BD3cXisVertbc%3D 10751453
40. D Mouginot BH Gahwiler 1995 Characterization of synaptic connections between cortex and deep nuclei of the rat cerebellum in vitro Neuroscience 64 3 699 712 1:CAS:528:DyaK2MXjt1Kksrg%3D 7715782
41. K Alvina K Khodakhah 2008 Selective regulation of spontaneous activity of neurons of the deep cerebellar nuclei by N-type calcium channels in juvenile rats J Physiol 586 10 2523 2538 1:CAS:528:DC%2BD1cXmsFOhtLw%3D 18372310
42. SS Feng D Jaeger 2008 The role of SK calcium-dependent potassium currents in regulating the activity of deep cerebellar nucleus neurons: a dynamic clamp study Cerebellum 7 4 542 546 1:CAS:528:DC%2BD1cXhsFSrurvM 18985424
43. VG Shakkottai CH Chou S Oddo CA Sailer HG Knaus GA Gutman, et al. 2004 Enhanced neuronal excitability in the absence of neurodegeneration induces cerebellar ataxia J Clin Invest 113 4 582 590 1:CAS:528:DC%2BD2cXhsFKhsbk%3D 14966567
44. R Muri T Knopfel 1994 Activity induced elevations of intracellular calcium concentration in neurons of the deep cerebellar nuclei J Neurophysiol 71 1 420 428 1:STN:280:DyaK2c3htVShsw%3D%3D 8158239
45. EC Hurlock M Bose G Pierce RH Joho 2009 Rescue of motor coordination by Purkinje cell-targeted restoration of Kv3.3 channels in Kcnc3-null mice requires Kcnc1 J Neurosci 29 50 15735 15744 1:CAS:528:DC%2BD1MXhs1WhtbfI 20016089
46. H Jahnsen 1986 Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro J Physiol 372 129 147 1:STN:280:DyaL283ltlyqsg%3D%3D 3723407 (Pubitemid 16048146)
47. S Chen DE Hillman 1993 Colocalization of neurotransmitters in the deep cerebellar nuclei J Neurocytol 22 2 81 91 1:CAS:528:DyaK3sXisVyhs74%3D 8095297
48. MW Bagnall B Zingg A Sakatos SH Moghadam HU Zeilhofer S Lac 2009 Glycinergic projection neurons of the cerebellum J Neurosci 29 32 10104 10110 1:CAS:528:DC%2BD1MXhtVWktr3E 19675244
49. M Uusisaari T Knopfel 2010 GlyT2+ neurons in the lateral cerebellar nucleus Cerebellum 9 42 55 19826891
50. ZF Mainen TJ Sejnowski 1996 Influence of dendritic structure on firing pattern in model neocortical neurons Nature 382 6589 363 366 1:CAS:528:DyaK28Xks1Wnsr0%3D 8684467
51. R Quadroni T Knopfel 1994 Compartmental models of type A and type B guinea pig medial vestibular neurons J Neurophysiol 72 4 1911 1924 1:STN:280:DyaK2M7itlCiuw%3D%3D 7529823
52. K Alvina G Ellis-Davies K Khodakhah 2009 T-type calcium channels mediate rebound firing in intact deep cerebellar neurons Neuroscience 158 2 635 641 1:CAS:528:DC%2BD1MXns12jsQ%3D%3D 18983899
53. E Perez-Reyes LL Cribbs A Daud AE Lacerda J Barclay MP Williamson, et al. 1998 Molecular characterization of a neuronal low-voltage-activated T-type calcium channel Nature 391 6670 896 900 1:CAS:528:DyaK1cXhsFylu7g%3D 9495342
54. JH Lee AN Daud LL Cribbs AE Lacerda A Pereverzev U Klockner, et al. 1999 Cloning and expression of a novel member of the low voltage-activated T-type calcium channel family J Neurosci 19 6 1912 1921 1:CAS:528:DyaK1MXhslKnt74%3D 10066244
55. JE McRory CM Santi KS Hamming J Mezeyova KG Sutton DL Baillie, et al. 2001 Molecular and functional characterization of a family of rat brain T-type calcium channels J Biol Chem 276 6 3999 4011 1:CAS:528:DC%2BD3MXht1Ggurs%3D 11073957
56. BE McKay JE McRory ML Molineux J Hamid TP Snutch GW Zamponi, et al. 2006 Ca(V)3 T-type calcium channel isoforms differentially distribute to somatic and dendritic compartments in rat central neurons Eur J NeuroSci 24 9 2581 2594 17100846
57. D Kim I Song S Keum T Lee MJ Jeong SS Kim, et al. 2001 Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca(2+) channels Neuron 31 1 35 45 1:CAS:528:DC%2BD3MXlsFKksrY%3D 11498049
58. S Lee TH Han PM Sonner JE Stern PD Ryu SY Lee 2008 Molecular characterization of T-type Ca(2+) channels responsible for low threshold spikes in hypothalamic paraventricular nucleus neurons Neuroscience 155 4 1195 1203 1:CAS:528:DC%2BD1cXhtVKlsLfJ 18657597
59. M Iftinca J Hamid L Chen D Varela R Tadayonnejad C Altier, et al. 2007 Regulation of T-type calcium channels by Rho-associated kinase Nat Neurosci 10 7 854 860 1:CAS:528:DC%2BD2sXmvFKmsLg%3D 17558400
60. KS Wilcox MJ Gutnick GR Christoph 1988 Electrophysiological properties of neurons in the lateral habenula nucleus: an in vitro study J Neurophysiol 59 1 212 225 1:STN:280:DyaL1c7ktVylug%3D%3D 3343602
61. JR Pugh IM Raman 2008 Mechanisms of potentiation of mossy fiber EPSCs in the cerebellar nuclei by coincident synaptic excitation and inhibition J Neurosci 28 42 10549 10560 1:CAS:528:DC%2BD1cXht1ymt7vN 18923031
62. V Gauck M Thomann D Jaeger A Borst 2001 Spatial distribution of low- and high-voltage-activated calcium currents in neurons of the deep cerebellar nuclei J Neurosci 21 15 RC158 1:STN:280:DC%2BD3Mvhslegtw%3D%3D 11459879
63. JH Lee JC Gomora LL Cribbs E Perez-Reyes 1999 Nickel block of three cloned T-type calcium channels: low concentrations selectively block alpha1H Biophys J 77 6 3034 3042 1:CAS:528:DyaK1MXotVGhsLc%3D 10585925
64. M Iftinca BE McKay TP Snutch JE McRory RW Turner GW Zamponi 2006 Temperature dependence of T-type calcium channel gating Neuroscience 142 4 1031 1042 1:CAS:528:DC%2BD28XhtFCjsLfP 16935432
65. AD Randall RW Tsien 1997 Contrasting biophysical and pharmacological properties of T-type and R-type calcium channels Neuropharmacology 36 7 879 893 1:CAS:528:DyaK2sXkvFClsbc%3D 9257934
66. IM Raman BP Bean 1999 Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons J Neurosci 19 5 1663 1674 1:CAS:528:DyaK1MXhtlCrtrw%3D 10024353
67. RH Joho EC Hurlock 2009 The role of Kv3-type potassium channels in cerebellar physiology and behavior Cerebellum 8 323 333 1:CAS:528: DC%2BD1MXhtVGjurfF 19247732
68. V Alonso-Espinaco I Elezgarai J Diez-Garcia N Puente T Knopfel P Grandes 2008 Subcellular localization of the voltage-gated potassium channels Kv3.1b and Kv3.3 in the cerebellar dentate nucleus of glutamic acid decarboxylase 67-green fluorescent protein transgenic mice Neuroscience 155 4 1059 1069 1:CAS:528:DC%2BD1cXhtVKlsLbP 18682278
69. MR Smith AB Nelson S Du Lac 2002 Regulation of firing response gain by calcium-dependent mechanisms in vestibular nucleus neurons J Neurophysiol 87 4 2031 2042 11929921
70. + signaling Science 314 5799 615 620 1:CAS:528:DC%2BD28XhtFeitr7K 17068255
71. 2+ channels in hippocampal neurons Nature 395 6705 900 905 1:CAS:528:DyaK1cXntlKjt7Y%3D 9804423
72. 2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites Nat Neurosci 11 6 683 692 1:CAS:528:DC%2BD1cXmtlCisbg%3D 18488023
73. C Jimenez E Bourinet V Leuranguer S Richard TP Snutch J Nargeot 2000 Determinants of voltage-dependent inactivation affect Mibefradil block of calcium channels Neuropharmacology 39 1 1 10 1:CAS:528:DyaK1MXnvFejuro%3D 10665814
74. FS Afshari K Ptak ZM Khaliq TM Grieco NT Slater DR McCrimmon, et al. 2004 Resurgent Na currents in four classes of neurons of the cerebellum J Neurophysiol 92 5 2831 2843 1:CAS:528:DC%2BD2cXpvFahsLw%3D 15212420
75. M Ghamari-Langroudi CW Bourque 2002 Flufenamic acid blocks depolarizing afterpotentials and phasic firing in rat supraoptic neurones J Physiol 545 Pt 2 537 542 1:CAS:528:DC%2BD3sXktFyitg%3D%3D 12456832
76. 2+ release from internal stores: role in generating depolarizing after-potentials in rat supraoptic neurones J Physiol 498 Pt 2 339 350 1:CAS:528:DyaK2sXhtFCls7o%3D 9032683
77. P Telgkamp IM Raman 2002 Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei J Neurosci 22 19 8447 8457 1:CAS:528:DC%2BD38Xns1Cju7o%3D 12351719
78. M Palkovits E Mezey J Hamori J Szentagothai 1977 Quantitative histological analysis of the cerebellar nuclei in the cat. I. Numerical data on cells and on synapses Exp Brain Res 28 1-2 189 209 1:STN:280: DyaE2s3isFChuw%3D%3D 881003
79. M Garwicz CF Ekerot H Jorntell 1998 Organizational principles of cerebellar neuronal circuitry News Physiol Sci 13 26 32 11390755
80. P Telgkamp DE Padgett VA Ledoux CS Woolley IM Raman 2004 Maintenance of high-frequency transmission at Purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites Neuron 41 1 113 126 1:CAS:528:DC%2BD2cXnt12lsw%3D%3D 14715139
81. JR Pugh IM Raman 2005 GABAA receptor kinetics in the cerebellar nuclei: evidence for detection of transmitter from distant release sites Biophys J 88 3 1740 1754 1:CAS:528:DC%2BD2MXis1Whtb4%3D 15626699
82. BR Sastry W Morishita S Yip T Shew 1997 GABA-ergic transmission in deep cerebellar nuclei Prog Neurobiol 53 2 259 271 1:CAS:528:DyaK2sXnt12gtrw%3D 9364613
83. SL Shin E De Schutter 2006 Dynamic synchronization of Purkinje cell simple spikes J Neurophysiol 96 6 3485 3491 16987931
84. E De Schutter V Steuber 2009 Patterns and pauses in Purkinje cell simple spike trains: experiments, modeling and theory Neuroscience 162 3 816 826 19249335
85. CM Pedroarena C Schwarz 2003 Efficacy and short-term plasticity at GABAergic synapses between Purkinje and cerebellar nuclei neurons J Neurophysiol 89 2 704 715 1:CAS:528:DC%2BD3sXhslKqu70%3D 12574448
86. CI De Zeeuw AS Berrebi 1995 Postsynaptic targets of Purkinje cell terminals in the cerebellar and vestibular nuclei of the rat Eur J NeuroSci 7 11 2322 2333 8563981
87. CI de Zeeuw AS Berrebi 1996 Individual Purkinje cell axons terminate on both inhibitory and excitatory neurons in the cerebellar and vestibular nuclei Ann N Y Acad Sci 781 607 610 8694453
88. KJ Staley BL Soldo WR Proctor 1995 Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors Science 269 5226 977 981 1:CAS:528:DyaK2MXnsFOmtLY%3D 7638623
89. D Billups D Attwell 2002 Control of intracellular chloride concentration and GABA response polarity in rat retinal ON bipolar cells J Physiol 545 Pt 1 183 198 1:CAS:528:DC%2BD3sXktFertA%3D%3D 12433959
90. KE Gavrikov JE Nilson AV Dmitriev CL Zucker SC Mangel 2006 Dendritic compartmentalization of chloride cotransporters underlies directional responses of starburst amacrine cells in retina Proc Natl Acad Sci USA 103 49 18793 18798 1:CAS:528:DC%2BD28XhtlahtbzP 17124178
91. - transport J Physiol 519 Pt 3 693 712 1:CAS:528:DyaK1MXmslGjsbg%3D 10457084
92. F Saitow M Murano H Suzuki 2009 Modulatory effects of serotonin on GABAergic synaptic transmission and membrane properties in the deep cerebellar nuclei J Neurophysiol 101 3 1361 1374 1:CAS:528:DC%2BD1MXktFCnsL0%3D 19144744
93. NJ Woolf LL Butcher 1989 Cholinergic systems in the rat brain: IV. Descending projections of the pontomesencephalic tegmentum Brain Res Bull 23 6 519 540 1:STN:280:DyaK3c7itl2isg%3D%3D 2611694
94. Y Takeuchi H Kimura Y Sano 1982 Immunohistochemical demonstration of serotonin-containing nerve fibers in the cerebellum Cell Tissue Res 226 1 1 12 1:CAS:528:DyaL38XlslGksro%3D 6751545 (Pubitemid 13238361)
95. L Olson K Fuxe 1971 On the projections from the locus coeruleus noradrealine neurons: the cerebellar innervation Brain Res 28 1 165 171 1:STN:280:DyaE3M3ltFWgug%3D%3D 4104275
96. JC Schwartz JM Arrang M Garbarg H Pollard M Ruat 1991 Histaminergic transmission in the mammalian brain Physiol Rev 71 1 1 51 1:CAS:528: DyaK3MXlsFSns7s%3D 1846044
97. D Mouginot BH Gahwiler 1996 Presynaptic GABAB receptors modulate IPSPs evoked in neurons of deep cerebellar nuclei in vitro J Neurophysiol 75 2 894 901 1:CAS:528:DyaK28Xhs1ejs70%3D 8714662
98. W Morishita BR Sastry 1995 Pharmacological characterization of pre- and postsynaptic GABAB receptors in the deep nuclei of rat cerebellar slices Neuroscience 68 4 1127 1137 1:CAS:528:DyaK2MXotlWhs7Y%3D 8544987
99. CM Pedroarena S Kamphausen 2008 Glycinergic synaptic currents in the deep cerebellar nuclei Neuropharmacology 54 5 784 795 1:CAS:528:DC%2BD1cXjs1Slur0%3D 18234240
100. W Zhang DJ Linden 2006 Long-term depression at the mossy fiber-deep cerebellar nuclear synapse J Neuroscience 26 6935 6944 1:CAS:528: DC%2BD28XmvVGqtrY%3D
101. V Gauck D Jaeger 2003 The contribution of NMDA and AMPA conductances to the control of spiking in neurons of the deep cerebellar nuclei J Neurosci 23 22 8109 8118 1:CAS:528:DC%2BD3sXnt1WqtLc%3D 12954873
102. T Knopfel 2007 Two new non-competitive mGlu1 receptor antagonists are potent tools to unravel functions of this mGlu receptor subtype Br J Pharmacol 151 6 723 724 1:STN:280:DC%2BD2svhtVKntQ%3D%3D 17502846
103. N Zheng IM Raman 2010 Synaptic inhibition, excitation, and plasticity in neurons of the cerebellar nuclei Cerebellum 9 56 66 19847585
104. FM Dreyfus A Tscherter AC Errington JJ Renger HS Shin VN Uebele, et al. 2010 Selective T-type calcium channel block in thalamic neurons reveals channel redundancy and physiological impact of I(T)window J Neurosci 30 1 99 109 1:CAS:528:DC%2BC3cXmtVeqsg%3D%3D 20053892
105. H Straka N Vibert PP Vidal LE Moore MB Dutia 2005 Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity Prog Neurobiol 76 6 349 392 1:CAS:528:DC%2BD2MXht1arsL7O 16263204
106. RC Lambert T Bessaih N Leresche 2006 Modulation of neuronal T-type calcium channels CNS Neurol Disord Drug Targets 5 6 611 627 1:CAS:528: DC%2BD28Xht1GntLvM 17168746
107. AJ Becker J Pitsch D Sochivko T Opitz M Staniek CC Chen, et al. 2008 Transcriptional upregulation of Cav3.2 mediates epileptogenesis in the pilocarpine model of epilepsy J Neurosci 28 49 13341 13353 1:CAS:528: DC%2BD1cXhsV2murzE 19052226
108. M Uusisaari T Knopfel 2008 GABAergic synaptic communication in the GABAergic and non-GABAergic cells in the deep cerebellar nuclei Neuroscience 156 3 537 549 1:CAS:528:DC%2BD1cXht1egu77F 18755250
109. AJ Hansen 1985 Effect of anoxia on ion distribution in the brain Physiol Rev 65 1 101 148 1:CAS:528:DyaL2MXhtFSksL4%3D 3880896
110. JE Lisman 1997 Bursts as a unit of neural information: making unreliable synapses reliable Trends Neurosci 20 1 38 43 1:CAS:528:DyaK2sXhtlyhsQ%3D%3D 9004418
111. MJ Chacron A Longtin L Maler 2004 To burst or not to burst? J Comput Neurosci 17 2 127 36 15306735
112. SM Sherman 2001 Tonic and burst firing: dual modes of thalamocortical relay Trends Neurosci 24 2 122 126 1:CAS:528:DC%2BD3MXntlylsQ%3D%3D 11164943
113. HJ Alitto TG Weyand WM Usrey 2005 Distinct properties of stimulus-evoked bursts in the lateral geniculate nucleus J Neurosci 25 2 514 523 1:CAS:528:DC%2BD2MXptV2hsw%3D%3D 15647497
114. NA Lesica GB Stanley 2004 Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus J Neurosci 24 47 10731 10740 1:CAS:528:DC%2BD2cXhtVKls7%2FL 15564591
115. AM Oswald MJ Chacron B Doiron J Bastian L Maler 2004 Parallel processing of sensory input by bursts and isolated spikes J Neurosci 24 18 4351 4362 1:CAS:528:DC%2BD2cXktFCjtL8%3D 15128849
116. EE Fanselow K Sameshima LA Baccala MA Nicolelis 2001 Thalamic bursting in rats during different awake behavioral states Proc Natl Acad Sci USA 98 26 15330 15335 1:CAS:528:DC%2BD38XpsVCq 11752471
117. NA Lesica C Weng J Jin CI Yeh JM Alonso GB Stanley 2006 Dynamic encoding of natural luminance sequences by LGN bursts PLoS Biol 4 7 e209 16756389
118. W Metzner C Koch R Wessel F Gabbiani 1998 Feature extraction by burst-like spike patterns in multiple sensory maps J Neurosci 18 6 2283 2300 1:CAS:528:DyaK1cXhs1ylsbc%3D 9482813
119. AM Oswald B Doiron L Maler 2007 Interval coding. I. Burst interspike intervals as indicators of stimulus intensity J Neurophysiol 97 4 2731 2743 17409176
120. Bengtsson FL, Carl-Fredrik E, Jorntell H (2008) Convergence of Purkinje cell synaptic input to deep cerebellar nuclear neurons in vivo. Proc Soc Neurosci, Washington
121. JM Delgado-Garcia A Gruart 2006 Building new motor responses: eyelid conditioning revisited Trends Neurosci 29 6 330 338 1:CAS:528: DC%2BD28XlvFGgsLs%3D 16713636
122. K Ohtsuka H Noda 1995 Discharge properties of Purkinje cells in the oculomotor vermis during visually guided saccades in the macaque monkey J Neurophysiol 74 5 1828 1840 1:STN:280:DyaK287ltVyqug%3D%3D 8592177
123. K Ohtsuka H Noda 1992 Burst discharges of mossy fibers in the oculomotor vermis of macaque monkeys during saccadic eye movements Neurosci Res 15 1-2 102 114 1:STN:280:DyaK3s7jtlCnug%3D%3D 1336577
124. M Ouardouz BR Sastry 2000 Mechanisms underlying LTP of inhibitory synaptic transmission in the deep cerebellar nuclei J Neurophysiol 84 3 1414 1421 1:CAS:528:DC%2BD3cXmslehtrw%3D 10980014