Frequency-dependent reliability of spike propagation is function of axonal voltage-gated sodium channels in cerebellar purkinje cells

Cerebellum

Volumn 12, Issue 6, 2013, Pages 862-869

  Yang, Zhilai ^a,b   Wang, Jin Hui ^a,b  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

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

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE ENDING; NERVE FIBER; NERVE FUNCTION; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PURKINJE CELL; RAT; RELIABILITY; SIGNAL TRANSDUCTION; SODIUM CURRENT; SPIKE FREQUENCY; SPIKE PROPAGATION; SPIKE WAVE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; AXONS; BIOPHYSICS; BIOTIN; CEREBELLUM; CNIDARIAN VENOMS; ELECTRIC STIMULATION; NERVE NET; PATCH-CLAMP TECHNIQUES; PURKINJE CELLS; RATS; RATS, WISTAR; SODIUM CHANNEL BLOCKERS; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84892441266     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-013-0499-2     Document Type: Article

References (52)

1. Debanne D, Campanac E, Bialowas A, Carlier E, Alcaraz G. Axon physiology. Physiological Review. 2011;91:555-602.
2. Wu KY, Zhou XP, Luo ZG. Geranylgeranyltransferase I is essential for dendritic development of cerebellar Purkinje cells. Mol Brain. 2010;3:18.
3. Clark BA, Monsivais P, Branco T, London M, Hausser M. The site of action potential initiation in cerebellar Purkinje neurons. Nat Neurosci. 2005;8:137-9.
4. Colbert CM, Pan E. Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci. 2002;5:533-8.
5. Coombs JS, Curtis DR, Eccles JC. The interpretation of spike potentials of motoneurones. J Physiol Lond. 1957;139:198-231.
6. Davie JT, Clark BA, Hausser M. The origin of the complex spike in cerebellar Purkinje cells. J Neurosci. 2008;28:7599-609.
7. Fuortes MGF, Frank K, Becker MC. Steps in the production of motor neuron spikes. J Gen Physiol. 1957;40:735-52.
8. Hausser M, Stuart G, Racca C, Sakmann B. Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron. 1995;15:637-47.
9. Hu W, Tian C, Li T, Yang P, Hou H, Shu YS. Distinct contribution of Nav1.6 and Nav1.2 in action potential initiation and backpropagation. Nat Neurosci. 2009;12:996-1002.
10. Kole MHP, Ilschner SU, Kampa BM, Williams SR, Ruben PC, Stuart GJ. Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci. 2008;11:178-86.
11. Kuba H, Ishii TM, Ohmori H. Axonal site of spike initiation enhances auditory coincidence detection. Nature. 2006;444:1069-72.
12. Meeks JP, Mennerick S. Action potential initiation and propagation in CA3 pyramidal axons. J Neurophysiol. 2007;97:3460-72.
13. Palmer LM, Clark BA, Grundemann J, Roth A, Stuart GJ, Hausser M. Initiation of simple and complex spikes in cerebellar Purkinje cells. J Physiol Lond. 2010;588:1709-17.
14. Chen N, Yu J, Qian H, Ge R, Wang JH. Axons amplify somatic incomplete spikes into uniform amplitudes in mouse cortical pyramidal neurons. PLoS One. 2010;5(7):e11868.
15. Engel D, Jonas P. Presynaptic action potential amplification by voltage-gated Na+ channels in hippocampal mossy fiber boutons. Neuron. 2005;45:405-17.
16. Chakrabarti L, Eng J, Ivanov N, Garden GA, La Spada AR. Autophagy activation and enhanced mitophagy characterize the Purkinje cells of pcd mice prior to neuronal death. Mol Brain. 2009;2:24.
17. Hodgkin AL, Huxley AF. Propagation of electrical signals along giant nerve fibers. Proc R Soc Lond B Biol Sci. 1952;140:177-83.
18. Huxley AF, Stampfli R. Evidence for saltatory conduction in peripheral myelinated nerve fibres. J Physiol Lond. 1949;108:315-39.
19. Khaliq ZM, Raman IM. Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons. J Neurosci. 2005;25:454-63.
20. Monsivais P, Clark BA, Roth A, Hausser M. Determinants of action potential propagation in cerebellar Purkinje cell axons. J Neurosci. 2005;25:464-72.
21. Stuart G, Spruston N, Sakmann B, Hausser M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 1997;20:125-31.
22. Debanne D, Guerineau NC, Gahwiler BH, Thompson SM. Actionpotential propagation gated by an axonal I(A)-like K+ conductance in hippocampus. Nature. 1997;389:286-9.
23. Khaliq ZM, Raman IM. Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. J Neurosci. 2006;26:1935-44.
24. Meeks JP, Mennerick S. Selective effects of potassium elevations on glutamate signaling and action potential conduction in hippocampus. J Neurosci. 2004;24:197-206.
25. Debanne D. Information processing in the axon. Nat Rev Neurosci. 2004;5:304-16.
26. Eccles JC, Sasaki K, Strata P. Interpretation of the potential fields generated in the cerebellar cortex by a mossy fibre volley. Exp Brain Res. 1967;3:58-80.
27. Harvey RJ, Porter R, Rawson JA. The natural discharges of Purkinje cells in paravermal regions of lobules V and VI of the monkey's cerebellum. J Physiol Lond. 1977;271:515-36.
28. Llinas R, Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol Lond. 1980;305:171-95.
29. Aldrich RW, Corey DP, Stevens CF. A reinterpretation of mammalian sodium channel gating based on single channel recording. Nature. 1983;306:436-41.
30. Chen N, Chen X, Yu J, Wang J-H. After-hyperpolarization improves spike programming through lowering threshold potentials and refractory periods mediated by voltage-gated sodium channels. Biochem Biophys Res Commun. 2006;346:938-45.
31. Goldman L. Stationarity of sodium channel gating kinetics in excised patches from neuroblastoma N1E 115. Biophys J. 1995; 69:2364-8.
32. Chen N, Chen X, Wang J-H. Homeostasis established by coordination of subcellular compartment plasticity improves spike encoding. J Cell Sci. 2008;121:2961-71.
33. Ge R, Qian H, Wang JH. Physiological synaptic signals initiate sequential spikes at soma of cortical pyramidal neurons. Mol Brain. 2011;4:19.
34. Wang J-H. Short-term cerebral ischemia causes the dysfunction of interneurons and more excitation of pyramidal neurons. Brain Res Bull. 2003;60:53-8.
35. Yu J, Qian H, Wang JH. Upregulation of transmitter release probability improves a conversion of synaptic analogue signals into neuronal digital spikes. Mol Brain. 2012;5:26.
36. Zhang F, Liu B, Lei Z, Wang J. mGluR1,5 activation improves network asynchrony and GABAergic synapse attenuation in the amygdala: implication for anxiety-like behavior in DBA/2 mice. Mol Brain. 2012;5:20.
37. Chen N, Zhu Y, Gao X, Guan S, Wang J-H. Sodium channelmediated intrinsic mechanisms underlying the differences of spike programming among GABAergic neurons. Biochem Biophys Res Commun. 2006;346:281-7.
38. Hockberger PE, Tseng H-Y, Connor JA. Development of rat cerebellar Purkinje cells: electrophysiological properties following acute isolation and in long-term culture. J Neurosci. 1989; 9:2258-71.
39. McKay BE, Turner RW. Physiological and morphological development of the rat cerebellar Purkinje cell. J Physiol Lond. 2005;567:829-50.
40. Qi Y et al. Intracellular Ca2+ regulates spike encoding at cortical GABAergic neurons and cerebellar Purkinje cells differently. Biochem Biophys Res Commun. 2009;381:129-33.
41. Jaeger D, Bower JM. Prolonged responses in rat cerebellar Purkinje cells following activation of the granule cell layer: an intracellular in vitro and in vivo investigation. Exp Brain Res. 1994;100:200-14.
42. Loewenstein Y, Mahon S, Chadderton P, Kitamura K, Sompolinsky H, Yarom Y, et al. Bistability of cerebellar Purkinje cells modulated by sensory stimulation. Nat Neurosci. 2005;8:202-11.
43. Wang JH, Wei J, Chen X, Yu J, Chen N, Shi J. The gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding. J Cell Sci. 2008;121:2951-60.
44. Yu J, Qian H, Chen N, Wang JH. Quantal glutamate release is essential for reliable neuronal encodings in cerebral networks. PLoS One. 2011;6:e25219.
45. Zhang G, Gao Z, Guan S, Zhu Y, Wang JH. Upregulation of excitatory neurons and downregulation of inhibitory neurons in barrel cortex are associated with loss of whisker inputs. Mol Brain. 2013;6:2.
46. Zhao J, Wang D, Wang J-H. Barrel cortical neurons and astrocytes coordinately respond to an increased whisker stimulus frequency. Mol Brain. 2012;5(1):10.
47. Mantegazza M, Franceschetti S, Avanzini G. Anemone toxin (ATX II)-induced increase in persistent sodium current: effects on the firing properties of rat neocortical pyramidal neurones. J Physiol Lond. 1998;507(Pt 1):105-16.
48. Rathmayer W. Anemone toxin discriminates between ionic channels for receptor potential and for action potential production in a sensory neuron. Neurosci Lett. 1979;13:313-8.
49. Wang J-H, Kelly PT. Ca2+/CaM signalling pathway up-regulates glutamatergic synaptic function in non-pyramidal fast-spiking neurons of hippocampal CA1. J Physiol Lond. 2001;533:407-22.
50. Mackenzie PJ, Umemiya M, Murphy TH. Ca2+ imaging of CNS axons in culture indicates reliable coupling between single action potentials and distal functional release sites. Neuron. 1996;16:783-95.
51. Foust A, Popovic M, Zecevic D, McCormick DA. Action potentials initiate in the axon initial segment and propagate through axon collaterals reliably in cerebellar Purkinje neurons. J Neurosci. 2010;30:6891-902.
52. Wang JH, Yang Z, Qian H, Chen N. Functional compatibility between Purkinje cell axon branches and their target neurons in the cerebellum. Biophys J. 2013;104:330a.