Essential role of axonal VGSC inactivation in time-dependent deceleration and unreliability of spike propagation at cerebellar Purkinje cells

Molecular Brain

Volumn 7, Issue 1, 2014, Pages

  Yang, Zhilai ^a,c,d   Gu, Erwei ^d   Lu, Xianfu ^d   Wang, Jin Hui ^a,b,c  

^a INSTITUTE OF BIOPHYSICS   (China)

^b QINGDAO UNIVERSITY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^d ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

Action potential; Axon; Cerebellum; Neuron; Purkinje cell; Spike propagation

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; BRAIN SLICE; CEREBELLUM; CONTROLLED STUDY; DECELERATION; ENZYME INACTIVATION; FACILITATION; NERVE CELL MEMBRANE POTENTIAL; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; SPIKE WAVE; VELOCITY;

ACTION POTENTIALS; ANIMALS; AXONS; CEREBELLUM; CNIDARIAN VENOMS; ION CHANNEL GATING; PURKINJE CELLS; RATS; RATS, WISTAR; TIME FACTORS; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84891808767     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-7-1     Document Type: Article

References (77)

1. Axon physiology. Debanne D, Campanac E, Bialowas A, Carlier E, Alcaraz G, Physiol Rev 2011 91 555 602 10.1152/physrev.00048.2009 21527732
2. Elementary interactions between neurons: synaptic transmission. Kandel ER, Siegelbaum SA, Schwartz JH, Principles of neural science New York: McGraw-Hill, Kandel ER, Schwartz JH, Jessell TM, 3 2000 175 308
3. Synaptic transmission. Shepherd GM, Neurobiology New York: Oxford University Press, Shepherd GM, 4 1998
4. The gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding. Wang JH, Wei J, Chen X, Yu J, Chen N, Shi J, J Cell Sci 2008 121 2951 2960 10.1242/jcs.025684 18697836
5. Quantal glutamate release is essential for reliable neuronal encodings in cerebral networks. Yu J, Qian H, Chen N, Wang JH, PLoS ONE 2011 6 25219 10.1371/journal.pone.0025219 21949885
6. The site of action potential initiation in cerebellar Purkinje neurons. Clark BA, Monsivais P, Branco T, London M, Hausser M, Nat Neurosci 2005 8 137 139 10.1038/nn1390 15665877 (Pubitemid 40194039)
7. Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Colbert CM, Pan E, Nat Neurosci 2002 5 533 538 10.1038/nn0602-857 11992119 (Pubitemid 34568994)
8. The interpretation of spike potentials of motoneurones. Coombs JS, Curtis DR, Eccles JC, J Physiol 1957 139 198 231 13492209
9. The origin of the complex spike in cerebellar Purkinje cells. Davie JT, Clark BA, Hausser M, J Neurosci 2008 28 7599 7609 10.1523/JNEUROSCI.0559-08.2008 18650337
10. Steps in the production of motor neuron spikes. Fuortes MGF, Frank K, Becker MC, J Gen Physiol 1957 40 735 752 10.1085/jgp.40.5.735 13428986
11. Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Hausser M, Stuart G, Racca C, Sakmann B, Neuron 1995 15 637 647 10.1016/0896-6273(95)90152-3 7546743
12. Distinct contribution of Nav1.6 and Nav1.2 in action potential initiation and backpropagation. Hu W, Tian C, Li T, Yang P, Hou H, Shu YS, Nat Neurosci 2009 12 996 1002 10.1038/nn.2359 19633666
13. Involvement of persistent Na + current in spike initiation in primary sensory neurons of the rat mesencephalic trigeminal nucleus. Kang Y, Saito M, Sato H, Toyoda H, Maeda Y, Hirai T, Bae YC, J Neurophysiol 2007 97 2385 2393 10.1152/jn.01191.2006 17229822 (Pubitemid 46411168)
14. Action potential generation requires a high sodium channel density in the axon initial segment. Kole MHP, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ, Nat Neurosci 2008 11 178 186 10.1038/nn2040 18204443 (Pubitemid 351170500)
15. Axonal site of spike initiation enhances auditory coincidence detection. Kuba H, Ishii TM, Ohmori H, Nature 2006 444 1069 1072 10.1038/nature05347 17136099 (Pubitemid 46018526)
16. Is action potential threshold lowest in the axon? Maarten H, Kole P, Stuart GJ, Nat Neurosci 2008 11 1253 1255 10.1038/nn.2203 18836442
17. Action potential initiation and propagation in CA3 pyramidal axons. Meeks JP, Mennerick S, J Neurophysiol 2007 97 3460 3472 10.1152/jn.01288.2006 17314237 (Pubitemid 47084761)
18. Initiation of simple and complex spikes in cerebellar Purkinje cells. Palmer LM, Clark BA, Grundemann J, Roth A, Stuart GJ, Hausser M, J Physiol 2010 588 1709 1717 10.1113/jphysiol.2010.188300 20351049
19. Axons amplify somatic incomplete spikes into uniform amplitudes in mouse cortical pyramidal neurons. Chen N, Yu J, Qian H, Ge R, Wang JH, PLoS ONE 2010 5 7 11868 10.1371/journal.pone.0011868 20686619
20. Presynaptic action potential amplification by voltage-gated Na + channels in hippocampal mossy fiber boutons. Engel D, Jonas P, Neuron 2005 45 405 417 10.1016/j.neuron.2004.12.048 15694327 (Pubitemid 40188208)
21. Propagation of electrical signals along giant nerve fibers. Hodgkin AL, Huxley AF, Proc R Soc Lond B Biol Sci 1952 140 177 183 10.1098/rspb.1952.0054 13003922
22. Evidence for saltatory conduction in peripheral myelinated nerve fibres. Huxley AF, Stampfli R, J Physiol 1949 108 315 339
23. Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. Khaliq ZM, Raman IM, J Neurosci 2005 25 454 463 10.1523/JNEUROSCI.3045- 04.2005 15647489 (Pubitemid 40105616)
24. Determinants of action potential propagation in cerebellar Purkinje cell axons. Monsivais P, Clark BA, Roth A, Hausser M, J Neurosci 2005 25 464 472 10.1523/JNEUROSCI.3871-04.2005 15647490 (Pubitemid 40105617)
25. Beyond faithful conduction: short-term dynamics, neuromodulation, and long-term regulation of spike propagation in the axon. Bucher D, Goaillard JM, Prog Neurobiol 2011 94 307 346 10.1016/j.pneurobio.2011.06.001 21708220
26. Action-potential propagation gated by an axonal I (A)-like K + conductance in hippocampus. Debanne D, Guerineau NC, Gahwiler BH, Thompson SM, Nature 1997 389 286 289 10.1038/38502 9305843 (Pubitemid 27406642)
27. Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. Khaliq ZM, Raman IM, J Neurosci 2006 26 1935 1944 10.1523/JNEUROSCI.4664-05.2006 16481425
28. Selective effects of potassium elevations on glutamate signaling and action potential conduction in hippocampus. Meeks JP, Mennerick S, J Neurosci 2004 24 197 206 10.1523/JNEUROSCI.4845-03.2004 14715952 (Pubitemid 38181684)
29. Information processing in the axon. Debanne D, Nat Rev Neurosci 2004 5 304 316 10.1038/nrn1397 15034555 (Pubitemid 38478657)
30. Interpretation of the potential fields generated in the cerebellar cortex by a mossy fibre volley. Eccles JC, Sasaki K, Strata P, Exp Brain Res 1967 3 58 80 6031000
31. The natural discharges of Purkinje cells in paravermal regions of lobules V and VI of the monkey's cerebellum. Harvey RJ, Porter R, Rawson JA, J Physiol 1977 271 515 536 411917 (Pubitemid 8213327)
32. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. Llinas R, Sugimori M, J Physiol 1980 305 171 195 7441552 (Pubitemid 10048155)
33. A reinterpretation of mammalian sodium channel gating based on single channel recording. Aldrich RW, Corey DP, Stevens CF, Nature 1983 306 436 441 10.1038/306436a0 6316158 (Pubitemid 14235560)
34. After-hyperpolarization improves spike programming through lowering threshold potentials and refractory periods mediated by voltage-gated sodium channels. Chen N, Chen X, Yu J, Wang J-H, Biochem Biophys Res Commun 2006 346 938 945 10.1016/j.bbrc.2006.06.003 16777065
35. Stationarity of sodium channel gating kinetics in excised patches from neuroblastoma N1E 115. Goldman L, Biophysics Journal 1995 69 2364 2368 10.1016/S0006-3495(95)80105-0
36. Physiological synaptic signals initiate sequential spikes at soma of cortical pyramidal neurons. Ge R, Qian H, Wang JH, Mol Brain 2011 4 19 10.1186/1756-6606-4-19 21549002
37. Electrophysiological properties of pyramidal neurons in the rat prefrontal cortex: an in vivo intracellular recording study. Deqenetais E, Thierry AM, Glowinski J, Gioanni Y, Cereb Cortex 2002 12 1 16 10.1093/cercor/12.1.1 11734528 (Pubitemid 33152013)
38. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. Haider B, Duque A, Hasenstaub A, McCormick DA, J Neurosci 2006 26 4535 4545 10.1523/JNEUROSCI.5297-05.2006 16641233 (Pubitemid 44315353)
39. Action potential threshold of hippocampal pyramidal cells in vivo is increased by recent spiking activity. Henze DA, Buzsaki G, Neuroscience 2001 105 121 130 10.1016/S0306-4522(01)00167-1 11483306 (Pubitemid 32722099)
40. Reprint of "frequency tuning and firing pattern properties of auditory thalamic neurons: an in vivo intracellular recording from the guinea pig" Zhang Z, Yu YQ, Liu CH, Chan YS, He J, Neuroscience 2008 154 273 282 10.1016/S0306-4522(08)00741-0 18555163 (Pubitemid 351802247)
41. The refractory periods and threshold potentials of sequential spikes measured by whole-cell recordings. Chen N, Chen SL, Wu YL, Wang JH, Biochem Biophys Res Commun 2006 340 151 157 10.1016/j.bbrc.2005.11.170 16343428 (Pubitemid 41827660)
42. Sodium channel-mediated intrinsic mechanisms underlying the differences of spike programming among GABAergic neurons. Chen N, Zhu Y, Gao X, Guan S, Wang J-H, Biochem Biophys Res Commun 2006 346 281 287 10.1016/j.bbrc.2006.05.120 16756951 (Pubitemid 43865995)
43. Prolonged responses in rat cerebellar Purkinje cells following activation of the granule cell layer: an intracellular in vitro and in vivo investigation. Jaeger D, Bower JM, Exp Brain Res 1994 100 200 214 7813659 (Pubitemid 24253650)
44. Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y, Hausser M, Nat Neurosci 2005 8 202 211 10.1038/nn1393 15665875 (Pubitemid 40194051)
45. Anemone toxin (ATX II)-induced increase in persistent sodium current: effects on the firing properties of rat neocortical pyramidal neurones. Mantegazza M, Franceschetti S, Avanzini G, J Physiol 1998 507 Pt 1 105 116 9490824 (Pubitemid 28102679)
46. Anemone toxin discriminates between ionic channels for receptor potential and for action potential production in a sensory neuron. Rathmayer W, Neurosci Lett 1979 13 313 318 10.1016/0304-3940(79)91512-X 43492 (Pubitemid 9248491)
47. Re-evaluation of the action potential upstroke velocity as a measure of the Na + current in cardiac myocytes at physiological conditions. Berecki G, Wilders R, de Jonge B, van Ginneken AC, Verkerk AO, PLoS ONE 2010 5 15772 10.1371/journal.pone.0015772 21217835
48. Overlap syndrome of cardiac sodium channel disease in mice carrying the equivalent mutation of human SCN5A-1795insD. Remme CA, Verkerk AO, Nuyens D, van Ginneken AC, van Brunschot S, Belterman CN, Wilders R, van Roon MA, Tan HL, Wilde AA, et al. Circulation 2006 114 2584 2594 10.1161/CIRCULATIONAHA.106. 653949 17145985 (Pubitemid 44967341)
49. The cerebellar network: from structure to function and dynamics. D'Angelo E, Mazzarello P, Prestori F, Mapelli J, Solinas S, Lombardo P, Cesana E, Gandolfi D, Congi L, Brain Res Rev 2011 66 5 15 10.1016/j.brainresrev.2010.10. 002 20950649
50. Action potentials initiate in the axon initial segment and propagate through axon collaterals reliably in cerebellar Purkinje neurons. Foust A, Popovic M, Zecevic D, McCormick DA, J Neurosci 2010 30 6891 6902 10.1523/JNEUROSCI.0552-10.2010 20484631
51. Projection of reconstructed single Purkinje cell axons in relation to the cortical and nuclear aldolase C compartments of the rat cerebellum. Sugihara I, Fujita H, Na J, Quy PN, Li BY, Ikeda D, J Comp Neurol 2009 512 282 304 10.1002/cne.21889 19003905
52. Cytosolic phospholipase A2 alpha/arachidonic acid signaling mediates depolarization-induced suppression of excitation in the cerebellum. Wang DJ, Yang D, Su LD, Xie YJ, Zhou L, Sun CL, Wang Y, Wang XX, Shen Y, PLoS ONE 2012 7 41499 10.1371/journal.pone.0041499 22927908
53. Interneurons of the neocortical inhibitory system. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silbergerg G, Wu C, Nature Review of Neuroscience 2004 5 793 807 10.1038/nrn1519 (Pubitemid 39336216)
54. Activity-dependent competition regulates motor neuron axon pathfinding via PlexinA3. Plazas PV, Nicol X, Spitzer NC, Proc Natl Acad Sci U S A 2013 110 1524 1529 10.1073/pnas.1213048110 23302694
55. Functional classification of neurons in the mouse lateral cerebellar nuclei. Uusisaari M, Knopfel T, Cerebellum 2011 10 637 646 10.1007/s12311-010- 0240-3 21116763
56. Functional compatibility between Purkinje cell axon branches and their target neurons in the cerebellum. Wang JH, Yang Z, Qian H, Chen N, Biophys J 2013 104 330a
57. Homeostasis established by coordination of subcellular compartment plasticity improves spike encoding. Chen N, Chen X, Wang J-H, J Cell Sci 2008 121 2961 2971 10.1242/jcs.022368 18697837
58. Sodium channel Na (v)1.6 is localized at nodes of ranvier, dendrites, and synapses. Caldwell JH, Schaller KL, Lasher RS, Peles E, Levinson SR, Proc Natl Acad Sci U S A 2000 97 5616 5620 10.1073/pnas.090034797 10779552 (Pubitemid 30313767)
59. Incomplete inactivation and rapid recovery of voltage-dependent sodium channels during high-frequency firing in cerebellar Purkinje neurons. Carter BC, Bean BP, J Neurophysiol 2011 105 860 871 10.1152/jn.01056.2010 21160003
60. Dynamic compartmentalization of the voltage-gated sodium channels in axons. Garrido JJ, Fernandes F, Moussif A, Fache MP, Giraud P, Dargent B, Biol Cell 2003 95 437 445 10.1016/S0248-4900(03)00091-1 14597261 (Pubitemid 37441634)
61. Expression and distribution of voltage-gated sodium channels in the cerebellum. Schaller KL, Caldwell JH, Cerebellum 2003 2 2 9 10.1080/ 14734220309424 12882229 (Pubitemid 38281797)
62. Diverse functions and dynamic expression of neuronal sodium channels. Waxman SG, Cummins TR, Black JA, Dib-Hajj S, Novartis Found Symp 2002 241 34 60 11771649
63. Postsynaptic injection of Ca2+/CaM induces synaptic potentiation requiring CaM-KII and PKC activity. Wang JH, Kelly PT, Neuron 1995 15 443 452 10.1016/0896-6273(95)90048-9 7646896
64. Balance between postsynaptic Ca2 + -dependent protein kinase and phosphatase activities controlling synaptic strength. Wang J-H, Kelly PT, Learn Mem 1996 3 170 181 10.1101/lm.3.2-3.170 10456087 (Pubitemid 26357742)
65. Postsynaptic calcineurin activity down-regulates synaptic transmission by weakening intracellular Ca2+ signaling mechanisms in hippocampal CA1 neurons. Wang J-H, Kelly PT, J Neurosci 1997 17 4600 4611 9169521 (Pubitemid 27246918)
66. Calcium signal-dependent plasticity of neuronal excitability developed postnatally. Zhang M, Hung F, Zhu Y, Xie Z, Wang J, J Neurobiol 2004 61 277 287 10.1002/neu.20045 15382030 (Pubitemid 39426152)
67. Ca2+ imaging of CNS axons in culture indicates reliable coupling between single action potentials and distal functional release sites. Mackenzie PJ, Umemiya M, Murphy TH, Neuron 1996 16 783 795 10.1016/S0896-6273(00)80098-7 8607996
68. Real-time neuronal homeostasis by coordinating VGSC intrinsic properties. Ge R, Chen N, Wang JH, Biochem Biophys Res Commun 2009 387 585 589 10.1016/j.bbrc.2009.07.066 19616515
69. Short-term cerebral ischemia causes the dysfunction of interneurons and more excitation of pyramidal neurons. Wang J-H, Brain Res Bull 2003 60 53 58 10.1016/S0361-9230(03)00026-1 12725892 (Pubitemid 36506452)
70. Upregulation of transmitter release probability improves a conversion of synaptic analogue signals into neuronal digital spikes. Yu J, Qian H, Wang JH, Mol Brain 2012 5 26 10.1186/1756-6606-5-26 22852823
71. Development of rat cerebellar purkinje cells: electrophysiological properties following acute isolation and in long-term culture. Hockberger PE, Tseng H-Y, Connor JA, J Neurosci 1989 9 2258 2271 2746328 (Pubitemid 19193559)
72. Physiological and morphological development of the rat cerebellar Purkinje cell. McKay BE, Turner RW, J Physiol Lond 2005 567 Pt3 829 850 16002452 (Pubitemid 41387829)
73. Intracellular Ca2+ regulates spike encoding at cortical GABAergic neurons and cerebellar Purkinje cells differently. Qi Y, Huang L, Ni H, Zhou X, Zhang J, Zhu Y, Ge M, Guan S, Wang JH, Biochem Biophys Res Commun 2009 381 129 133 10.1016/j.bbrc.2009.02.058 19351606
74. Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Stuart G, Hausser M, Neuron 1994 13 703 712 10.1016/0896-6273(94)90037-X 7917300 (Pubitemid 24300174)
75. Differential modulation of glutamatergic and cholinergic synapses by calcineurin in hippocampal CA1 fast-spiking interneurons. Wang JH, Zhang M, Brain Res 1004 125 135
76. High threshold, proximal initiation, and slow conduction velocity of action potentials in dentate granule neuron mossy fibers. Kress GJ, Dowling MJ, Meeks JP, Mennerick S, J Neurophysiol 2008 100 281 291 10.1152/jn.90295.2008 18480368
77. Ca2+/CaM signalling pathway up-regulates glutamatergic synaptic function in non-pyramidal fast-spiking neurons of hippocampal CA1. Wang J-H, Kelly PT, J Physiol Lond 2001 533 407 422 10.1111/j.1469-7793.2001.0407a.x 11389201 (Pubitemid 32519997)