Voltage-gated K+ channels contributing to temporal precision at the inner hair cell-auditory afferent nerve fiber synapses in the mammalian cochlea

다국어 초록 (Multilingual Abstract)

To perform auditory tasks such as soundlocalization in the space, auditory neurons in the brain mustdistinguish sub-millisecond temporal differences in signalsfrom two ears. Such high temporal resolution is possiblewhen each neuron in the ascending auditory pathway firesbrief action potential at very accurate timing. Various preandpostsynaptic machineries ensuring such high temporalprecision of auditory synaptic transmission have beenidentified. Of particular, in this review, the role of K?channels in shortening the duration of synaptic potentialswill be discussed. First, the contribution of K? channels toAP firing of general auditory neurons will be discussed.
Then, the focus will be moved to the inner hair cell (IHC)-auditory afferent nerve fiber (ANF) synapses, the firstsynapses of ascending auditory pathway. Molecular andimmunohistological techniques have revealed various K?channels in the cell bodies and their processes of ANFs.
Since the development of patch-clamp recordings from theANF dendrites in 2002, it became possible to monitor theIHC-ANF synaptic transmission in greater detail. Asrevealed in brain auditory synapses, several different K?channels appear to participate in reducing the duration ofsynaptic potentials at the IHC-ANF synapses. In addition,K? channels at the ANF dendrites might act as potentialtargets of efferent feedback from the brain. The hypothesisis that, upon loud sound exposure, efferent neurotransmittersreleased onto the ANF dendrites activate certain K?channels and prevent excitotoxicity of ANFs. Therefore,K? channels of the ANF dendrites might provide potential sites of pharmacological actions to prevent noise-inducedhearing loss.

참고문헌 (Reference)

1 Hossain, W.A., "Where is the spike generator of the cochlear nerve? Voltage-gated sodium channels in the mouse cochlea" 25 : 6857-6868, 2005

2 Cao, X.J., "Voltage-sensitive conductances of bushy cells of the mammalian ventral cochlear nucleus" 97 : 3961-3975, 2007

3 Chen, W.C., "Voltage-gated and two-poredomain potassium channels in murine spiral ganglion neurons" 222 : 89-99, 2006

4 Rennie, K.J., "Voltage-dependent currents in isolated vestibular afferent calyx terminals" 95 : 26-32, 2006

5 Grant, L., "Two modes of release shape the postsynaptic response at the inner hair cell ribbon synapse" 30 : 4210-4220, 2010

6 Glowatzki, E., "Transmitter release at the hair cell ribbon synapse" 5 : 147-154, 2002

7 Hopkins, W.F., "Toxin and subunit specificity of blocking affinity of three peptide toxins for heteromultimeric, voltage-gated potassium channels expressed in Xenopus oocytes" 285 : 1051-1060, 1998

8 Gardner, S.M., "Time course and permeation of synaptic AMPA receptors in cochlear nuclear neurons correlate with input" 19 : 8721-8729, 1999

9 Ryugo, D.K., "The projections of intracellularly labeled auditory nerve fibers to the dorsal cochlear nucleus of cats" 329 : 20-35, 1993

10 Honore, E., "The neuronal background K2P channels : Focus on TREK1" 8 : 251-261, 2007

11 Shin, H.W., "The inhibitory effects of bupivacaine, levobupivacaine, and ropivacaine on K(two-pore domain potassium)channel TREK-1" 28 : 81-86, 2013

12 Schneggenburger, R., "The calyx of Held" 326 : 311-337, 2006

13 Fuchs, P.A., "The afferent synapse of cochlear hair cells" 13 : 452-458, 2003

14 Golding, N.L., "Synaptic integration in dendrites : Exceptional need for speed" 590 : 5563-5569, 2012

15 Ferragamo, M.J., "Synaptic inputs to stellate cells in the ventral cochlear nucleus" 79 : 51-63, 1998

16 Chagot, B., "Solution structure of APETx2, a specific peptide inhibitor of ASIC3 proton-gated channels" 14 : 2003-2010, 2005

17 Kaczmarek, L.K., "Slack, slick and sodium-activated potassium channels" 2013 (2013): 354262-, 2013

18 Yang, B., R., "Slack and slick K(Na)channels regulate the accuracy of timing of auditory neurons" 27 : 2617-2627, 2007

19 Goutman, J.D., "Short-term facilitation modulates size and timing of the synaptic response at the inner hair cell ribbon synapse" 31 : 7974-7981, 2011

20 Darrow, "Selective removal of lateral olivocochlear efferents increases vulnerability to acute acoustic injury" 97 : 1775-1785, 2007

21 Brew, H.M., "Seizures and reduced life span in mice lacking the potassium channel subunit Kv1. 2, but hypoexcitability and enlarged Kv1 currents in auditory neurons" 98 : 1501-1525, 2007

22 Tong, H., "Regulation of Kv channel expression and neuronal excitability in rat medial nucleus of the trapezoid body maintained in organotypic culture" 588 : 1451-1468, 2010

23 Tong, H., "Protection from noise-induced hearing loss by Kv2. 2 potassium currents in the central medial olivocochlear system" 33 : 9113-9121, 2013

24 Bal, R., "Potassium currents in octopus cells of the mammalian cochlear nucleus" 86 : 2299-2311, 2001

25 Kanjhan, R., "Postnatal changes in TASK-1 and TREK-1 expression in rat brain stem and cerebellum" 15 : 1321-1324, 2004

26 Yang, B., "Pharmacological activation and inhibition of slack(Slo2. 2)channels" 51 : 896-906, 2006

27 Li, S., "Pathogenic plasticity of Kv7.2/3 channel activity is essential for the induction of tinnitus" 9980-9985, 2013

28 Macica, C.M., "Modulation of the Kv3. 1b potassium channel isoform adjusts the fidelity of the firing pattern of auditory neurons" 23 : 1133-1141, 2003

29 Song, P., "Modulation of Kv3. 1b potassium channel phosphorylation in auditory neurons by conventional and novel protein kinase C isozymes" 281 : 15582-15591, 2006

30 Karcz, A., "Low-voltage activated Kv1. 1subunits are crucial for the processing of sound source location in the lateral superior olive in mice" 589 : 1143-1157, 2011

31 Lv, P., "Kv7-type channel currents in spiral ganglion neurons : Involvement in sensorineural hearing loss" 285 : 34699-34707, 2010

32 Johnston, J., "Kv4(Atype)potassium currents in the mouse medial nucleus of the trapezoid body" 27 : 1391-1399, 2008

33 Gittelman, J.X., "Kv1. 1-containing channels are critical for temporal precision during spike initiation" 96 : 1203-1214, 2006

34 Rothman, J.S., "Kinetic analyses of three distinct potassium conductances in ventral cochlear nucleus neurons" 89 : 3083-3096, 2003

35 Huang, H., "KCNQ5 channels control resting properties and release probability of a synapse" 14 : 840-847, 2011

36 Dhawan, R., "K? currents in isolated vestibular afferent calyx terminals" 11 : 463-476, 2010

37 Szabo, Z.S., "Ionic currents determining the membrane characteristics of type I spiral ganglion neurons of the guinea pig" 16 : 1887-1895, 2002

38 Hibino, H., "Inwardly rectifying potassium channels : Their structure, function, and physiological roles" 90 : 291-366, 2010

39 Goldstein, S.A., "International Union of Pharmacology. LV. Nomenclature and molecular relationships of two-P potassium channels" 57 : 527-540, 2005

40 Kubo, Y., "International Union of Pharmacology. LIV. Nomenclature and molecular relationships of inwardly rectifying potassium channels" 57 : 509-526, 2005

41 Gutman, G.A., "International Union of Pharmacology. LIII. Nomenclature and molecular relationships of voltagegated potassium channels" 57 : 473-508, 2005

42 Wei, A.D., "International Union of Pharmacology. LII. Nomenclature and molecular relationships of calcium-activated potassium channels" 57 : 463-472, 2005

43 Johnston, J., "Initial segment Kv2. 2 channels mediate a slow delayed rectifier and maintain high frequency action potential firing in medial nucleus of the trapezoid body neurons" 586 : 3493-3509, 2008

44 Oertel, D., "In the ventral cochlear nucleus Kv1. 1 and subunits of HCN1 are colocalized at surfaces of neurons that have low-voltage-activated and hyperpolarization-activated conductances" 154 : 77-86, 2008

45 Sokolowski, B.H., "Identification and localization of an arachidonic acid-sensitive potassium channel in the cochlea" 24 : 6265-6276, 2004

46 Brew, H.M., "Hyperexcitability and reduced low threshold potassium currents in auditory neurons of mice lacking the channel subunit Kv1. 1" 548 : 1-20, 2003

47 Liu, Q., "Heterogeneous intrinsic excitability of murine spiral ganglion neurons is determined by Kv1 and HCN channels" 257 : 96-110, 2014

48 Kiang, N.Y., "Hair-cell innervation by spiral ganglion cells in adult cats" 217 : 175-177, 1982

49 Khimich, D., "Hair cell synaptic ribbons are essential for synchronous auditory signalling" 434 : 889-894, 2005

50 Berglund, A.M., "Hair cell innervation by spiral ganglion neurons in the mouse" 255 : 560-570, 1987

51 Johnston, J., "Going native : Voltage-gated potassium channels controlling neuronal excitability" 588 : 3187-3200, 2010

52 Bhattacharjee, A., "For K? channels, Na? is the new Ca2?" 28 : 422-428, 2005

53 Adamson, C.L., "Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location" 447 : 331-350, 2002

54 Hibino, H., "Expression of an inwardly rectifying K? channel, Kir5. 1, in specific types of fibrocytes in the cochlear lateral wall suggests its functional importance in the establishment of endocochlear potential" 19 : 76-84, 2004

55 Fitzakerley, J.L., "Expression of Shal potassium channel subunits in the adult and developing cochlear nucleus of the mouse" 147 : 31-45, 2000

56 Jin, Z., "Expression and localization of K channels KCNQ2 and KCNQ3 in the mammalian cochlea" 14 : 98-105, 2009

57 Nie, L., M, "Expression and functional phenotype of mouse ERG K? channels in the inner ear : Potential role in K? regulation in the inner ear" 25 : 8671-8679, 2005

58 Hardman, R.M., "Ether-a-go-go-related gene K ?channels contribute to threshold excitability of mouse auditory brainstem neurons" 587 : 2487-2497, 2009

59 Maison, S.F., "Dopaminergic signaling in the cochlea : Receptor expression patterns and deletion phenotypes" 32 : 344-355, 2012

60 Jing, Z., "Disruption of the presynaptic cytomatrix protein bassoon degrades ribbon anchorage, multiquantal release, and sound encoding at the hair cell afferent synapse" 33 : 4456-4467, 2013

61 Grigg, J.J., "Differential expression of voltage-gated potassium channel genes in auditory nuclei of the mouse brainstem" 140 : 77-90, 2000

62 Rothman, J.S., "Differential expression of three distinct potassium currents in the ventral cochlear nucleus" 89 : 3070-3082, 2003

63 Beisel, K.W., "Differential expression of KCNQ4 in inner hair cells and sensory neurons is the basis of progressive high-frequency hearing loss" 25 : 9285-9293, 2005

64 Bortone, D.S., "Developmental time course of potassium channel expression in the rat cochlear nucleus" 211 : 114-125, 2006

65 Kanjhan, R., "Developmental expression of two-pore domain K? channels, TASK-1 and TREK-1, in the rat cochlea" 15 : 437-441, 2004

66 Simmons, D.D., "Development of the inner ear efferent system across vertebrate species" 53 : 228-250, 2002

67 Trussell, L.O., "Desensitization of AMPA receptors upon multiquantal neurotransmitter release" 10 : 1185-1196, 1993

68 Mo, Z.L., "Dendrotoxin-sensitive K(?)currents contribute to accommodation in murine spiral ganglion neurons" 542 : 763-778, 2002

69 Yi, E., "Dendritic voltage-gated ion channels shape postsynaptic potentials at the inner hair cell afferent synapses" Association for Research in Otolaryngology 2006

70 Yi, E., "Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea" 103 : 2532-2543, 2010

71 Kopp-Scheinpflug, C., "Decreased temporal precision of auditory signaling in Kcna1-null mice : An electrophysiological study in vivo" 23 : 199-207, 2003

72 Cui, Y.L., "Deafness associated changes in two-pore domain potassium channels in the rat inferior colliculus" 149 : 421-433, 2007

73 Holt, A.G., "Deafness associated changes in expression of two-pore domain potassium channels in the rat cochlear nucleus" 216–217 : 146-153, 2006

74 Mathews, P.J., "Control of submillisecond synaptic timing in binaural coincidence detectors by K(v)1 channels" 13 : 601-609, 2010

75 Wang, L.Y., "Contribution of the Kv3. 1 potassium channel to high-frequency firing in mouse auditory neurones" 509 (509): 183-194, 1998

76 Skinner, L.J., "Contribution of BK Ca2?-activated K? channels to auditory neurotransmission in the Guinea pig cochlea" 90 : 320-332, 2003

77 Darrow, K.N., "Cochlear efferent feedback balances interaural sensitivity" 9 : 1474-1476, 2006

78 Safieddine, S., "Choline acetyltransferase, glutamate decarboxylase, tyrosine hydroxylase, calcitonin gene-related peptide and opioid peptides coexist in lateral efferent neurons of rat and guinea-pig" 9 : 356-367, 1997

79 Trussell, L.O., "Cellular mechanisms for preservation of timing in central auditory pathways" 7 : 487-492, 1997

80 Lacas-Gervais, S., "BetaIVSigma1 spectrin stabilizes the nodes of Ranvier and axon initial segments" 166 : 983-990, 2004

81 Wersinger, E., "BK channels mediate cholinergic inhibition of high frequency cochlear hair cells" 5 : e13836-, 2010

82 Wang, W., "Association of the Kv1 family of K? channels and their functional blueprint in the properties of auditory neurons as revealed by genetic and functional analyses" 110 : 1751-1764, 2013

83 Zettel, M.L., "Agerelated decline in Kv3. 1b expression in the mouse auditory brainstem correlates with functional deficits in the medial olivocochlear efferent system" 8 : 280-293, 2007

84 Kujawa, S., "Adding insult to injury : Cochlear nerve degeneration after ‘‘temporary’’ noise-induced hearing loss" 29 : 14077-14085, 2009

85 Lu, Y., "Activitydependent regulation of the potassium channel subunits Kv1. 1and Kv3. 1" 470 : 93-106, 2004

86 Klug, A., "Activation and deactivation of voltage-dependent K? channels during synaptically driven action potentials in the MNTB" 96 : 1547-1555, 2006

87 Postlethwaite, M., "Acceleration of AMPA receptor kinetics underlies temperature-dependent changes in synaptic strength at the rat calyx of Held" 579 : 69-84, 2007

88 Kathiresan, T., "A protein interaction network for the large conductance Ca(2?)-activated K(?)channel in the mouse cochlea" 8 : 1972-1987, 2009