Hyperpolarization-activated current (Ih) in vestibular calyx terminals: Characterization and role in shaping postsynaptic events

JARO - Journal of the Association for Research in Otolaryngology

Volumn 13, Issue 6, 2012, Pages 745-758

  Meredith, Frances L ^a   Benke, Tim A ^a,b   Rennie, Katherine J ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Children's Hospital Colorado   (United States)

Author keywords

Balance; CAMP; Crista; Efferent; HCN channel

Indexed keywords

CYCLIC AMP; CYCLIC NUCLEOTIDE GATED CHANNEL;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ELECTRIC POTENTIAL; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; GERBIL; HAIR CELL; HYPERPOLARIZATION; MALE; MEMBRANE CONDUCTANCE; MEMBRANE STEADY POTENTIAL; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; SEMICIRCULAR CANAL; VESTIBULAR SYSTEM;

ACTION POTENTIALS; ANIMALS; CYCLIC AMP; CYCLIC GMP; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GERBILLINAE; HAIR CELLS, VESTIBULAR; ION CHANNELS; MALE; PYRIMIDINES;

EID: 84870422305     PISSN: 15253961     EISSN: 14387573     Source Type: Journal    
DOI: 10.1007/s10162-012-0342-3     Document Type: Article

References (54)

1. ATHANASIADES A, CLARK JW JR, GHORBEL F, BIDANI A (2000) An ionic current model for medullary respiratory neurons. J Comput Neurosci 9:237-257
2. AUTRET L, MECHALY I, SCAMPS F, VALMIER J, LORY P, DESMADRYL G (2005) The involvement of CaV3.2/α1H T-type calcium channels in excitability of mouse embryonic primary vestibular neurones. J Physiol 567:67-78
3. BAIRD RA, DESMADRYL G, FERNANDEZ C, GOLDBERG JM (1988) The vestibular nerve of the chinchilla. I. Peripheral innervation patterns in the horizontal and superior semicircular canals. J Neurophysiol 60:182-203
4. BAL R, OERTEL D (2000) Hyperpolarization-activated, mixed-cation current (I(h)) in octopus cells of the mammalian cochlear nucleus. J Neurophysiol 84:806-817
5. BIEL M, WAHL-SCHOTT C, MICHALAKIS S, ZONG X (2009) Hyperpolarization- activated cation channels: from genes to function. Physiol Rev 89:847-885
6. CHABBERT C, CHAMBARD JM, VALMIER J, SANS A, DESMADRYL G (1997) Voltage-activated sodium currents in acutely isolated mouse vestibular ganglion neurones. Neuroreport 8:1253-1256
7. CHABBERT C, CHAMBARD JM, SANS A, DESMADRYL G (2001a) Three types of depolarization-activated potassium currents in acutely isolated mouse vestibular neurons. J Neurophysiol 85:1017-1026
8. CHABBERT C, CHAMBARD JM, VALMIER J, SANS A, DESMADRYL G (2001b) Hyperpolarization-activated (Ih) current in mouse vestibular primary neurons. Neuroreport 12:2701-2704
9. CHAMBARD JM, CHABBERT C, SANS A, DESMADRYL G (1999) Developmental changes in low and high voltage-activated calcium currents in acutely isolated mouse vestibular neurons. J Physiol 518:141-149
10. CHEN C (1997) Hyperpolarization-activated current (Ih) in primary auditory neurons. Hear Res 110:179-190
11. CORREIA MJ, WOOD TG, PRUSAK D, WENG T, RENNIE KJ, WANG HQ (2004) Molecular characterization of an inward rectifier channel (IKir) found in avian vestibular hair cells: cloning and expression of pKir2.1. Physiol Genomics 19:155-169
12. DESMADRYL G, CHAMBARD JM, VALMIER J, SANS A (1997) Multiple voltage-dependent calcium currents in acutely isolated mouse vestibular ganglion neurons. Neuroscience 78:511-522
13. DHAWAN R, MANN SE, MEREDITH FL, RENNIE KJ (2010) K+ currents in isolated vestibular afferent calyx terminals. J Assoc Res Otolaryngol 11:463-476
14. DIBATTISTA M, MAZZATENTA A, GRASSI F, TIRINDELLI R, MENINI A (2008) Hyperpolarization-activated cyclic nucleotide-gated channels in mouse vomeronasal sensory neurons. J Neurophysiol 100:576-586
15. DIFRANCESCO D, TORTORA P (1991) Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 351:145-147
16. DRESCHER MJ, CHO WJ, FOLBE AJ, SELVAKUMAR D, KEWSON DT, ABUHAMDAN MD, OH CK, RAMAKRISHNAN NA, HATFIELD JS, KHAN KM, ANNE S, HARPOOL EC, DRESCHER DG (2010) An adenylyl cyclase signaling pathway predicts direct dopaminergic input to vestibular hair cells. Neuroscience 171:1054-1074
17. EATOCK RA, SONGER JE (2011) Vestibular hair cells and afferents: two channels for head motion signals. Annu Rev Neurosci 34:501-534
18. FRACE AM, MARUOKA F, NOMA A (1992) External K+ increases Na+ conductance of the hyperpolarization-activated current in rabbit cardiac pacemaker cells. Pflugers Arch 421:97-99
19. GÁBORJÁN A, LENDVAI B, VIZI ES (1999) Neurochemical evidence of dopamine release by lateral olivocochlear efferents and its presynaptic modulation in guinea-pig cochlea. Neuroscience 90:131-138
20. GARTHWAITE J (2008) Concepts of neural nitric oxide-mediated transmission. Eur J Neurosci 11:2783-2802
21. GOLDBERG JM (1996) Theoretical analysis of intercellular communication between the vestibular type I hair cell and its calyx ending. J Neurophysiol 76:1942-1957
22. GOLDBERG JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brian Res 130:277-297
23. HAGIWARA N, IRISAWA H (1989) Modulation by intracellular Ca2+ of the hyperpolarization-activated inward current in rabbit single sino-atrial node cells. J Physiol 409:121-141
24. HALTER JA, CLARK JW JR (1991) A distributed-parameter model of the myelinated nerve fiber. J Theor Biol 148:345-382
25. HARRIS NC, CONSTANTI A (1995) Mechanism of block by ZD 7288 of the hyperpolarization-activated inward rectifying current in guinea pig substantia nigra neurons in vitro. J Neurophysiol 74:2366-2378
26. HINES ML (1984) Efficient computation of branched nerve equations. Int J Bio-Med Computing 15:69-76
27. HOLT JR, EATOCK RA (1995) Inwardly rectifying currents of saccular hair cells from the leopard frog. J Neurophysiol 73:1484-1502
28. HOLT JC, LYSAKOWSKI A, GOLDBERG JM (2011) The efferent vestibular system. In: Ryugo DD, Fay RR, Popper AN (eds) Auditory and vestibular efferents. Springer, New York, pp 135-186
29. HORWITZ GC, LELLI A, GELEOC GS, HOLT JR (2010) HCN channels are not required for mechanotransduction in sensory hair cells of the mouse inner ear. PLoSone 5:1-7
30. HORWITZ GC, RISNER-JANICZEK JR, JONES SM, HOLT JR (2011) HCN channels in the inner ear are necessary for normal balance function. J Neurosci 31:16814-16825
31. HURLEY KM, GABOYARD S, ZHONG M, PRICE SD, WOOLTORTON JRA, LYSAKOWSKI A, EATOCK RA (2006) M-like K+ currents in type I hair cells and calyx afferent endings of the developing rat utricle. J Neurosci 40:10253-10269
32. IWASAKI S, CHIHARA Y, KOMUTA Y, ITO K, SAHARA Y (2008) Low-voltageactivated potassium channels underlie the regulation of intrinsic firing properties of rat vestibular ganglion cells. J Neurophysiol 100:2192-2204
33. KALLURI R, XUE J, EATOCK RA (2010) Ion channels set spike timing regularity of mammalian vestibular afferent neurons. J Neurophysiol 104:2034-2051
34. LIAO Z, LOCKHEAD D, LARSON ED, PROENZA C (2010) Phosphorylation and modulation of hyperpolarization-activated HCN4 channels by protein kinase A in the mouse sinoatrial node. J Gen Physiol 136:247-258
35. LIM R, KINDIG AE, DONNE SW, CALLISTER RJ, BRICHTA AM (2011) Potassium accumulation between type I hair cells and calyx terminals in mouse crista. Exp Brain Res 210:607-621
36. LIMÓN A, PÉREZ C, VEGA R, SOTO E (2005) Ca2+-activated K+-current density is correlated with soma size in rat vestibular-afferent neurons in culture. J Neurophysiol 94:3751-3761
37. LYNCH JW, BARRY PH (1991) Inward rectification in rat olfactory receptor neurons. Proc Biol Sci 243:149-153
38. LYSAKOWSKI A, GABOYARD-NIAY S, CALIN-JAGEMAN I, CHATLANI S, PRICE SD, EATOCK RA (2011) Molecular microdomains in a sensory terminal, the vestibular calyx ending. J Neurosci 31:10101-10114
39. MASETTO S, CORREIA MJ (1997) Electrophysiological properties of vestibular sensory and supporting cells in the labyrinth slice before and during regeneration. J Neurophysiol 78:1913-1927
40. MASETTO S, PERIN P, MALUSÀ A, ZUCCA G, VALLI P (2000) Membrane properties of chick semicircular canal hair cells in situ during embryonic development. J Neurophysiol 83:2740-2756
41. MCCUE MP, GUINAN JJ (1994) Influence of efferent stimulation on acoustically responsive vestibular afferents in the cat. J Neurosci 14:6071-6083
42. MEREDITH FL, LI G, RENNIE KJ (2011) Postnatal expression of an apamin-sensitive K(Ca) current in vestibular calyx terminals. J Memb Biol 244:81-91
43. MO Z-L, DAVIS RL (1997) Heterogeneous voltage dependence of inward rectifier currents in spiral ganglion neurons. J Neurophysiol 78:3019-3027
44. PROENZA C, ANGOLI D, AGRANOVICH E, MACRI V, ACCILI EA (2002) Pacemaker channels produce an instantaneous current. J Biol Chem 277:5101-5109
45. RENNIE KJ, CORREIA MJ (2000) Effects of cationic substitutions on delayed rectifier current in type I vestibular hair cells. J Membr Biol 173:139-148
46. RENNIE KJ, STREETER MA (2006) Voltage-dependent currents in isolated vestibular afferent calyx terminals. J Neurophysiol 95:26-32
47. RISNER JR, HOLT JR (2006) Heterogeneous potassium conductances contribute to the diverse firing properties of postnatal mouse vestibular ganglion neurons. J Neurophysiol 96:2364-2376
48. ROBERT A, HOWE JR (2003) How AMPA receptor desensitization depends on receptor occupancy. J Neurosci 23:847-858
49. RÜSCH A, EATOCK RA (1996) Voltage responses of mouse utricular hair cells to injected currents. Ann N Y Acad Sci 781:71-84
50. SCHWINDT PC, SPAIN WJ, CRILL WE (1992) Effects of intracellular calcium chelation on voltage-dependent and calcium-dependent currents in cat neocortical neurons. Neuroscience 47:571-578
51. VARGAS G, LUCERO MT (1999) Dopamine modulates inwardly rectifying hyperpolarization-activated current (Ih) in cultured rat olfactory receptor neurons. J Neurophysiol 81:149-159
52. WAHL-SCHOTT C, BIEL M (2009) HCN channels: structure, cellular regulation and physiological function. CellMol Life Sci 66:470-494
53. WAINGER BJ, DEGENNARO M, SANTORO B, SIEGELBAUM SA, TIBBS GR (2001) Molecular mechanisms of cAMP modulation of HCN pacemaker channels. Nature 411:805-810
54. YI E, ROUX I, GLOWATZKI E (2010) Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. J Neurophysiol 103:2532- 2543