Distinct roles for I T and I H in controlling the frequency and timing of rebound spike responses

Journal of Physiology

Volumn 589, Issue 22, 2011, Pages 5391-5413

  Engbers, Jordan D T ^a   Anderson, Dustin ^a   Tadayonnejad, Reza ^a   Mehaffey, W Hamish ^a   Molineux, Michael L ^a   Turner, Ray W ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL T TYPE; CYCLIC NUCLEOTIDE; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL FUNCTION; CEREBELLUM NUCLEUS; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ENZYME INACTIVATION; HYPERPOLARIZATION; MALE; NERVE CELL; NERVE CELL INHIBITION; NERVE EXCITABILITY; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SPIKE;

ANIMALS; ANIMALS, NEWBORN; CALCIUM CHANNELS, T-TYPE; CEREBELLAR NUCLEI; COMPUTER SIMULATION; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; FEMALE; MALE; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NEURONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 81255169975     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.215632     Document Type: Article

References (88)

1. Aizenman CD & Linden DJ (1999). Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. J Neurophysiol 82, 1697-1709.
2. Aizenman CD, Manis PB & Linden DJ (1998). Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse. Neuron 21, 827-835.
3. Alvina K, Ellis-Davies G & Khodakhah K (2009). T-type calcium channels mediate rebound firing in intact deep cerebellar neurons. Neuroscience 158, 635-641.
4. Alvina K, Walter JT, Kohn A, Ellis-Davies G & Khodakhah K (2008). Questioning the role of rebound firing in the cerebellum. Nat Neurosci 11, 1256-1258.
5. Babalyan AL & Fanardzhyan VV (1991). Electrophysiologic properties of red nucleus neurons in the rat brain slices. Neurophysiology 23, 454-461.
6. Bengtsson F, Ekerot CF & Jorntell H (2011). In vivo analysis of inhibitory synaptic inputs and rebounds in deep cerebellar nuclear neurons. PLoS One 6, e18822, 1-12.
7. Biel M, Wahl-Schott C, Michalakis S & Zong X (2009). Hyperpolarization-activated cation channels: from genes to function. Physiol Rev 89, 847-885.
8. Cattaneo A, Maffei L & Morrone C (1981). Two firing patterns in the discharge of complex cells encoding different attributes of the visual stimulus. Exp Brain Res 43, 115-118.
9. Czubayko U, Sultan F, Thier P & Schwarz C (2001). Two types of neurons in the rat cerebellar nuclei as distinguished by membrane potentials and intracellular fillings. J Neurophysiol 85, 2017-2029.
10. D'Angelo E & De Zeeuw CI (2009). Timing and plasticity in the cerebellum: focus on the granular layer. Trends Neurosci 32, 30-40.
11. De Schutter E & Steuber V (2009). Patterns and pauses in purkinje cell simple spike trains: experiments, modeling and theory. Neuroscience 162, 816-826.
12. De Zeeuw CI, Hoebeek FE, Bosman LW, Schonewille M, Witter L & Koekkoek SK (2011). Spatiotemporal firing patterns in the cerebellum. Nat Rev Neurosci 12, 327-344.
13. Dittman JS, Kreitzer AC & Regehr WG (2000). Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20, 1374-1385.
14. Doroshenko PA, Woppmann A, Miljanich G & Augustine GJ (1997). Pharmacologically distinct presynaptic calcium channels in cerebellar excitatory and inhibitory synapses. Neuropharmacology 36, 865-872.
15. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
16. Eggermont JJ (1998). Is there a neural code? Neurosci Biobehav Rev 22, 355-370.
17. 2+ channels - integration centers for neuronal signaling pathways. Trends Neurosci 29, 617-624.
18. Gardette R, Debono M, Dupont JL & Crepel F (1985a). Electrophysiological studies on the postnatal development of intracerebellar nuclei neurons in rat cerebellar slices maintained in vitro. I. Postsynaptic potentials. Brain Res 351, 47-55.
19. Gardette R, Debono M, Dupont JL & Crepel F (1985b). Electrophysiological studies on the postnatal development of intracerebellar nuclei neurons in rat cerebellar slices maintained in vitro. II. Membrane conductances. Brain Res 352, 97-106.
20. h) in spike-time precision and intrinsic resonance in cortical neurons in vitro. J Physiol 589, 3753-3773.
21. Gauck V & Jaeger D (2000). The control of rate and timing of spikes in the deep cerebellar nuclei by inhibition. J Neurosci 20, 3006-3016.
22. Gauck V & Jaeger D (2003). The contribution of NMDA and AMPA conductances to the control of spiking in neurons of the deep cerebellar nuclei. J Neurosci 23, 8109-8118.
23. Gauck V, Thomann M, Jaeger D & Borst A (2001). Spatial distribution of low- and high-voltage-activated calcium currents in neurons of the deep cerebellar nuclei. J Neurosci 21, RC158.
24. Heil P (2004). First-spike latency of auditory neurons revisited. Curr Opin Neurobiol 14, 461-467.
25. Hildebrand ME, Isope P, Miyazaki T, Nakaya T, Garcia E, Feltz A, Schneider T, Hescheler J, Kano M, Sakimura K, Watanabe M, Dieudonne S & Snutch TP (2009). Functional coupling between mGluR1 and Cav3.1 T-type calcium channels contributes to parallel fiber-induced fast calcium signaling within Purkinje cell dendritic spines. J Neurosci 29, 9668-9682.
26. Hoebeek FE, Witter L, Ruigrok TJ & De Zeeuw CI (2010). Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei. Proc Natl Acad Sci U S A 107, 8410-8415.
27. Huang Z, Lujan R, Kadurin I, Uebele VN, Renger JJ, Dolphin AC & Shah MM (2011). Presynaptic HCN1 channels regulate Cav3.2 activity and neurotransmission at select cortical synapses. Nat Neurosci 14, 478-486.
28. Huguenard JR (1996). Low-threshold calcium currents in central nervous system neurons. Annu Rev Physiol 58, 329-348.
29. Hurlock EC, Bose M, Pierce G & Joho RH (2009). Rescue of motor coordination by Purkinje cell-targeted restoration of Kv3.3 channels in Kcnc3-null mice requires Kcnc1. J Neurosci 29, 15735-15744.
30. Iftinca M, McKay BE, Snutch TP, McRory JE, Turner RW & Zamponi GW (2006). Temperature dependence of T-type calcium channel gating. Neuroscience 142, 1031-1042.
31. Jacobson GA, Lev I, Yarom Y & Cohen D (2009). Invariant phase structure of olivo-cerebellar oscillations and its putative role in temporal pattern generation. Proc Natl Acad Sci U S A 106, 3579-3584.
32. Jahnsen H (1986). Extracellular activation and membrane conductances of neurones in the guinea-pig deep cerebellar nuclei in vitro. J Physiol 372, 149-168.
33. Jahnsen H & Llinas R (1984). Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol 349, 227-247.
34. Kepecs A & Lisman J (2003). Information encoding and computation with spikes and bursts. Network 14, 103-118.
35. Kepecs A, Wang XJ & Lisman J (2002). Bursting neurons signal input slope. J Neurosci 22, 9053-9062.
36. Kisilevsky AE & Zamponi GW (2008). Presynaptic calcium channels: structure, regulators, and blockers. Handb Exp Pharmacol, 45-75.
37. h channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J Neurosci 26, 1677-1687.
38. Lee JH, Gomora JC, Cribbs LL & Perez-Reyes E (1999). Nickel block of three cloned T-type calcium channels: low concentrations selectively block α1H. Biophys J 77, 3034-3042.
39. Llinas R & Muhlethaler M (1988). Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brain stem-cerebellar preparation. J Physiol 404, 241-258.
40. McCormick DA & Pape HC (1990). Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol 431, 291-318.
41. McDonough SI & Bean BP (1998). Mibefradil inhibition of T-type calcium channels in cerebellar purkinje neurons. Mol Pharmacol 54, 1080-1087.
42. McKay BE, Engbers JD, Mehaffey WH, Gordon GR, Molineux ML, Bains JS & Turner RW (2007). Climbing fiber discharge regulates cerebellar functions by controlling the intrinsic characteristics of purkinje cell output. J Neurophysiol 97, 2590-2604.
43. Molineux ML, Fernandez FR, Mehaffey WH & Turner RW (2005). A-type and T-type currents interact to produce a novel spike latency-voltage relationship in cerebellar stellate cells. J Neurosci 25, 10863-10873.
44. Molineux ML, McRory JE, McKay BE, Hamid J, Mehaffey WH, Rehak R, Snutch TP, Zamponi GW & Turner RW (2006). Specific T-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons. Proc Natl Acad Sci U S A 103, 5555-5560.
45. Molineux ML, Mehaffey WH, Tadayonnejad R, Anderson D, Tennent AF & Turner RW (2008). Ionic factors governing rebound burst phenotype in rat deep cerebellar neurons. J Neurophysiol 100, 2684-2701.
46. Muri R & Knopfel T (1994). Activity induced elevations of intracellular calcium concentration in neurons of the deep cerebellar nuclei. J Neurophysiol 71, 420-428.
47. Ohyama T, Nores WL, Murphy M & Mauk MD (2003). What the cerebellum computes. Trends Neurosci 26, 222-227.
48. Orban G, Kiss T & Erdi P (2006). Intrinsic and synaptic mechanisms determining the timing of neuron population activity during hippocampal theta oscillation. J Neurophysiol 96, 2889-2904.
49. Oswald AM, Chacron MJ, Doiron B, Bastian J & Maler L (2004). Parallel processing of sensory input by bursts and isolated spikes. J Neurosci 24, 4351-4362.
50. Oswald AM, Doiron B & Maler L (2007). Interval coding. I. Burst interspike intervals as indicators of stimulus intensity. J Neurophysiol 97, 2731-2743.
51. Pedroarena CM (2010). Mechanisms supporting transfer of inhibitory signals into the spike output of spontaneously firing cerebellar nuclear neurons in vitro. Cerebellum 9, 67-76.
52. Pedroarena CM & Schwarz C (2003). Efficacy and short-term plasticity at GABAergic synapses between Purkinje and cerebellar nuclei neurons. J Neurophysiol 89, 704-715.
53. Perez-Reyes E (2003). Molecular physiology of low-voltage-activated T-type calcium channels. Physiol Rev 83, 117-161.
54. Person AL & Perkel DJ (2005). Unitary IPSPs drive precise thalamic spiking in a circuit required for learning. Neuron 46, 129-140.
55. Pugh JR & Raman IM (2006). Potentiation of mossy fiber EPSCs in the cerebellar nuclei by NMDA receptor activation followed by postinhibitory rebound current. Neuron 51, 113-123.
56. Pugh JR & Raman IM (2008). Mechanisms of potentiation of mossy fiber EPSCs in the cerebellar nuclei by coincident synaptic excitation and inhibition. J Neurosci 28, 10549-10560.
57. Raman IM, Gustafson AE & Padgett D (2000). Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci 20, 9004-9016.
58. Randall AD & Tsien RW (1997). Contrasting biophysical and pharmacological properties of T-type and R-type calcium channels. Neuropharmacology 36, 879-893.
59. Rowland NC & Jaeger D (2008). Responses to tactile stimulation in deep cerebellar nucleus neurons result from recurrent activation in multiple pathways. J Neurophysiol 99, 704-717.
60. Saitow F, Murano M & Suzuki H (2009). Modulatory effects of serotonin on GABAergic synaptic transmission and membrane properties in the deep cerebellar nuclei. J Neurophysiol 101, 1361-1374.
61. Sanchez-Alonso JL, Halliwell JV & Colino A (2008). ZD 7288 inhibits T-type calcium current in rat hippocampal pyramidal cells. Neurosci Lett 439, 275-280.
62. Sangrey T & Jaeger D (2010). Analysis of distinct short and prolonged components in rebound spiking of deep cerebellar nucleus neurons. Eur J Neurosci 32, 1646-1657.
63. Schneiderman N & Gormezano I (1964). Conditioning of the nictitating membrane of the rabbit as a function of Cs-Us interval. J Comp Physiol Psychol 57, 188-195.
64. Sherman SM (2001). Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci 24, 122-126.
65. + current mediated by the Kv4 channel regulates the generation of action potential in developing cerebellar granule cells. J Neurosci 20, 4145-4155.
66. Shin SL & De Schutter E (2006). Dynamic synchronization of Purkinje cell simple spikes. J Neurophysiol 96, 3485-3491.
67. Shin SL, Hoebeek FE, Schonewille M, De Zeeuw CI, Aertsen A & De Schutter E (2007). Regular patterns in cerebellar purkinje cell simple spike trains. PLoS One 2, e485, 1-9.
68. Smith MC (1968). CS-US interval and US intensity in classical conditioning of the rabbit's nictitating membrane response. J Comp Physiol Psychol 66, 679-687.
69. A receptors. Science 269, 977-981.
70. Steriade M, McCormick DA & Sejnowski TJ (1993). Thalamocortical oscillations in the sleeping and aroused brain. Science 262, 679-685.
71. Steuber V, Mittmann W, Hoebeek FE, Silver RA, De Zeeuw CI, Hausser M & De Schutter E (2007). Cerebellar LTD and pattern recognition by Purkinje cells. Neuron 54, 121-136.
72. Steuber V, Schultheiss NW, Silver RA, De Schutter E & Jaeger D (2011). Determinants of synaptic integration and heterogeneity in rebound firing explored with data-driven models of deep cerebellar nucleus cells. J Comput Neurosci 30, 633-658.
73. Tadayonnejad R, Anderson D, Molineux ML, Mehaffey WH, Jayasuriya K & Turner RW (2010). Rebound discharge in deep cerebellar nuclear neurons in vitro. Cerebellum 9, 352-374.
74. Tadayonnejad R, Mehaffey WH, Anderson D & Turner RW (2009). Reliability of triggering postinhibitory rebound bursts in deep cerebellar neurons. Channels 3, 1-7.
75. Telgkamp P, Padgett DE, Ledoux VA, Woolley CS & Raman IM (2004). Maintenance of high-frequency transmission at purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites. Neuron 41, 113-126.
76. Telgkamp P & Raman IM (2002). Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei. J Neurosci 22, 8447-8457.
77. Timmann D, Watts S & Hore J (1999). Failure of cerebellar patients to time finger opening precisely causes ball high-low inaccuracy in overarm throws. J Neurophysiol 82, 103-114.
78. 2+ spikes in distal dendrites of CA1 pyramidal neurons. Neuron 56, 1076-1089.
79. Uhlenbeck GE & Ornstein LS (1930). On the theory of the Brownian motion. Physical Review 36, 823-841.
80. A-receptor-mediated rebound burst firing and burst shunting in thalamus. J Neurophysiol 78, 1748-1751.
81. Uusisaari M & De Schutter E (2011). The mysterious microcircuitry of the cerebellar nuclei. J Physiol 589, 3441-357.
82. Uusisaari M & Knopfel T (2011). Functional classification of neurons in the mouse lateral cerebellar nuclei. Cerebellum (in press).
83. Uusisaari M, Obata K & Knopfel T (2007). Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei. J Neurophysiol 97, 901-911.
84. Zackowski KM, Thach WT Jr & Bastian AJ (2002). Cerebellar subjects show impaired coupling of reach and grasp movements. Exp Brain Res 146, 511-522.
85. Zamponi GW, Bourinet E & Snutch TP (1996). Nickel block of a family of neuronal calcium channels: subtype- and subunit-dependent action at multiple sites. J Membr Biol 151, 77-90.
86. Zhang W, Shin JH & Linden DJ (2004). Persistent changes in the intrinsic excitability of rat deep cerebellar nuclear neurons induced by EPSPs or IPSP bursts. J Physiol 561, 703-719.
87. Zheng N & Raman IM (2009). Ca currents activated by spontaneous firing and synaptic disinhibition in neurons of the cerebellar nuclei. J Neurosci 29, 9826-9838.
88. Zheng N & Raman IM (2011). Prolonged postinhibitory rebound firing in the cerebellar nuclei mediated by group I metabotropic glutamate receptor potentiation of L-type calcium currents. J Neurosci 31, 10283-10292.