Structural tuning and plasticity of the axon initial segment in auditory neurons

Journal of Physiology

Volumn 590, Issue 22, 2012, Pages 5571-5579

  Kuba, Hiroshi ^a,b  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; VOLTAGE GATED SODIUM CHANNEL;

ACOUSTIC NERVE FIBER; AUDITORY SYSTEM; BIRD; CELL FUNCTION; CELL SPECIFICITY; CELL STRUCTURE; CELL TYPE; COCHLEA; DENDRITE; HOMEOSTASIS; MAGNOCELLULAR NUCLEUS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOUND DETECTION; SPIKE; THALAMUS INTRALAMINAR NUCLEUS;

ANIMALS; AUDITORY PATHWAYS; AXONS; BASAL NUCLEUS OF MEYNERT; NEURONAL PLASTICITY; NEURONS;

EID: 84869741972     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.237305     Document Type: Review

References (70)

1. Araki T & Otani T (1955). Response of single motoneurons to direct stimulation in toad's spinal cord. J Neurophysiol 18, 472-485.
2. Atherton JF, Wokosin DL, Ramanathan S & Bevan MD (2008). Autonomous initiation and propagation of action potentials in neurons of the subthalamic nucleus. J Physiol 586, 5679-5700.
3. Bean BP (2007). The action potential in mammalian central neurons. Nat Rev Neurosci 8, 451-465.
4. Bender KJ & Trussell LO (2012). The physiology of the axon initial segment. Annu Rev Neurosci 35, 249-265.
5. Bliss TV & Lomo T (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. J Physiol 232, 331-356.
6. Bréchet A, Fache MP, Brachet A, Ferracci G, Baude A, Irondelle M, Pereira S, Leterrier C & Dargent B (2008). Protein kinase CK2 contributes to the organization of sodium channels in axonal membranes by regulating their interaction with ankyrin G. J Cell Biol 183, 1101-1114.
7. Carr CE & Boudreau RE (1991). Central projection of auditory nerve fibers in the barn owl. J Comp Neurol 314, 306-318.
8. Clark BD, Goldberg EM & Rudy B (2010). Electrogenic tuning of the axon initial segment. Neuroscientist 15, 651-668.
9. Colbert CM & Pan E (2002). Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci 5, 533-538.
10. Coombs JS, Curtis DR & Eccles JC (1957). The intepretation of spike potentials of motoneurons. J Physiol 139, 198-231.
11. Debanne D, Campanac E, Bialowas A, Carlier E & Alcaraz G (2011). Axon physiology. Physiol Rev 91, 461-508.
12. Dodson PD, Barker MC & Forsythe ID (2002). Two heteromeric Kv1 potassium channels differentially regulate action potential firing. J Neurosci 22, 6953-6961.
13. Duflocq A, Le Bras B, Bullier E, Couraud F & Davenne M (2008). Nav1.1 is predominantly expressed in nodes of Ranvier and axon initial segments. Mol Cell Neurosci 39, 180-192.
14. Dzhashiashvili Y, Zhan Y, Galinska J, Lam I, Grumet M & Salzer JL (2007). Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J Cell Biol 177, 857-870.
15. + influx between axon and soma. Nat Neurosci 13, 852-860.
16. Foust A, Popovic M, Zecevic D & McCormick DA (2010). Action potentials initiate in the axon initial segment and propagate through axon collaterals reliably in cerebellar Purkinje neurons. J Neurosci 30, 6891-6902.
17. Fried SI, Lasker AC, Desai NJ, Eddington DK & Rizzo JF 3rd (2009). Axonal sodium-channel bands shape the response to electric stimulation in retinal ganglion cells. J Neurophysiol 101, 1972-1987.
18. Fukui I & Ohmori H (2004). Tonotopic gradient of membrane and synaptic properties for neurons of the chicken nucleus magnocellularis. J Neurosci 24, 7514-7523.
19. Fukui I, Sato T & Ohmori H (2006). Improvement of phase information at low sound frequency in nucleus magnocellularis of the chicken. J Neurophysiol 96, 633-641.
20. Funabiki K, Ashida G & Konishi M (2012). Computation of interaural time difference in the owl's coincidence detector neurons. J Neurosci 31, 15245-15256.
21. + channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 58, 387-400.
22. Grubb MS & Burrone J (2010). Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 465, 1070-1074.
23. Grubb MS, Shu Y, Kuba H, Rasband MN, Wimmer VC & Bender KJ (2011). Short- and long-term plasticity at the axon initial segment. J Neurosci 31, 16049-16055.
24. Gulledge AT, Kampa BM & Stuart GJ (2005). Synaptic integration in dendritic trees. J Neurobiol 64, 75-90.
25. Hedstrom KL, Ogawa Y & Rasband MN (2008). AnkyrinG is required for maintenance of the axon initial segment and neuronal polarity. J Cell Biol 183, 635-640.
26. Hill KG, Stange G & Mo J (1989). Temporal synchronization in the primary auditory response in the pigeon. Hearing Res 39, 63-74.
27. v1.2 in action potential initiation and backpropagation. Nat Neurosci 12, 996-1002.
28. Inda MC, DeFelipe J & Munoz A (2006). Voltage-gated ion channels in the axon initial segment of human cortical pyramidal cells and their relationship with chandelier cells. Proc Natl Acad Sci U S A 103, 2920-2925.
29. Jenkins SM & Bennett V (2001). Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J Cell Biol 155, 739-746.
30. Jhaveri S & Morest DK (1982). Neuronal architecture in nucleus magnocellularis of the chicken auditory system with observations on nucleus laminaris: a light and electron microscope study. Neuroscience 7, 809-836.
31. Joris PX, Carney LH, Smith PH & Yin TCT (1994). Enhancement of neural synchronization in the anteroventral cochlear nucleus. I. Responses to tones at the characteristic frequency. J Neurophysiol 71, 1022-1036.
32. Kaphzan H, Buffington SA, Jung JI, Rasband MN & Klann E (2011). Alterations in intrinsic membrane properties and the axon initial segment in a mouse model of Angelman syndrome. J Neurosci 31, 17637-17648.
33. Khaliq ZM & Raman IM (2006). Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. J Neurosci 26, 1935-1944.
34. Kole MH, Ilschner SU, Kampa BM, Williams SR, Ruben PC & Stuart GJ (2008). Action potential generation requires a high sodium channel density in the axon initial segment. Nat Neurosci 11, 178-186.
35. Kole MH, Letzkus JJ & Stuart GJ (2007). Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55, 633-647.
36. Kole MHP & Stuart GJ (2012). Signal processing in the axon initial segment. Neuron 73, 235-247.
37. Konishi M (2003). Coding of auditory space. Annu Rev Neurosci 26, 31-55.
38. Köppl C (1994). Auditory nerve terminals in the cochlear nucleus magnocellularis: differences between low and high frequencies. J Comp Neurol 339, 438-446.
39. Köppl C (1997). Phase locking to high frequency in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. J Neurosci 17, 3312-3321.
40. G. A new ankyrin gene with neural-specific isoforms localized at the axon initial segment and node of Ranvier. J Biol Chem 270, 2352-2359.
41. Kress GJ, Dowling MJ, Eisenman LN & Mennerick S (2010). Axonal sodium channel distribution shapes the depolarized action potential threshold of dentate granule neurons. Hippocampus 20, 558-571.
42. Kuba H (2007). Cellular and molecular mechanisms of avian auditory coincidence detection. Neurosci Res 59, 370-376.
43. Kuba H, Ishii TM & Ohmori H (2006). Axonal site of spike initiation enhances auditory coincidence detection. Nature 444, 1069-1072.
44. Kuba H & Ohmori H (2009). Roles of axonal sodium channels in precise auditory time coding at nucleus magnocellularis of the chick. J Physiol 587, 87-100.
45. + channel distribution at the axon initial segment. Nature 465, 1075-1078.
46. Lorincz A & Nusser Z (2008). Cell-type-dependent molecular composition of the axon initial segment. J Neurosci 28, 14329-14340.
47. Lorincz A & Nusser Z (2010). Molecular identity of dendritic voltage-gated sodium channels. Science 328, 906-909.
48. Marder E & Prinz AA (2002). Modeling stability in neuron and network function: the role of activity in homeostasis. Bioessays 24, 1145-1154.
49. Meeks JP & Mennerick S (2007). Action potential initiation and propagation in CA3 pyramidal axons. J Neurophysiol 97, 3460-3472.
50. Ogawa Y & Rasband MN (2008). The functional organization and assembly of the axon initial segment. Curr Opin Neurobiol 18, 307-313.
51. Palay SL, Sotelo C, Peters A & Orkand PM (1968). The axon hillock and the initial segment. J Cell Biol 38, 193-201.
52. Palmer LM & Stuart GJ (2006). Site of action potential initiation in layer 5 pyramidal neurons. J Neurosci 26, 1854-1863.
53. Pan Z, Kao T, Horvath Z, Lemos J, Sul J-Y, Cranstoun SD, Bennett MV, Scherer SS & Cooper EC (2006). A common ankyrin-G-based mechanism retains KCNQ and Nav channels at electrically active domains of the axon. J Neurosci 26, 2599-2613.
54. Popovic MA, Foust AJ, McCormick DA & Zecevic D (2011). The spatio-temporal characteristics of action potential initiation in layer 5 pyramidal neurons: a voltage-imaging study. J Physiol 589, 4167-4187.
55. Rasband MN (2010). The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 11, 552-562.
56. v1.6 sodium channels in action potential initiation of CA1 pyramidal neurons. J Neurophysiol 100, 2361-2380.
57. Rubel EW & Parks TN (1975). Organization and development of the brain stem auditory nuclei of the chicken: tonotopic organization of n. magnocellularis and n. laminaris. J Comp Neurol 164, 411-434.
58. Schafer DP, Jha S, Liu F, Akella T, McCullough LD & Rasband MN (2009). Disruption of the axon initial segment cytoskeleton is a new mechanism for neuronal injury. J Neurosci 29, 13242-13254.
59. Schmidt-Hieber C & Bischofberger J (2010). Fast sodium channel gating supports localized and efficient axonal action potential initiation. J Neurosci 30, 10233-10242.
60. Shu Y, Duque A, Yu Y, Haider B & McCormick DA (2007a). Properties of action-potential initiation in neocortical pyramidal cells: evidence from whole-cell axon recording. J Neurophysiol 97, 746-760.
61. + current. Proc Natl Acad Sci U S A 104, 11453-11458.
62. Slee SJ, Higgs MH, Fairhall AL & Spain WJ (2010). Tonotopic tuning in a sound localization circuit. J Neurophysiol 103, 2857-2875.
63. Smith DJ & Rubel EW (1979). Organization and development of brain stem auditory nuclei of the chicken: dendritic gradient in nucleus laminaris. J Comp Neurol 186, 213-240.
64. Trunova S, Baek B & Giniger E (2011). Cdk5 regulates the size of an axon initial segment-like compartment in mushroom body neurons of the Drosophila central brain. J Neurosci 31, 10451-10462.
65. Trussell LO (1999) Synaptic mechanisms for coding timing in central auditory pathways. Annu Rev Physiol 61, 477-496.
66. Turrigiano GG & Nelson SB (2004). Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5, 97-107.
67. Vacher H, Yang JW, Cerda O, Autillo-Touati A, Dargent B & Trimmer JS (2011). Cdk-mediated phosphorylation of the Kvβ2 auxiliary subunit regulates Kv1 channel axonal targeting. J Cell Biol 192, 813-824.
68. Van Wart A, Trimmer JS & Matthews G (2007). Polarized distribution of ion channels within microdomains of the axon initial segment. J Comp Neurol 500, 339-352.
69. Wimmer VC, Reid CA, So EY, Berkovic SF & Petrou S (2010). Axon initial segment dysfunction in epilepsy. J Physiol 588, 1829-1840.
70. G is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol 143, 1295-1304.