Mechanotransduction and hyperpolarization-activated currents contribute to spontaneous activity in mouse vestibular ganglion neurons

Journal of General Physiology

Volumn 143, Issue 4, 2014, Pages 481-497

  Horwitz, Geoffrey C ^a,b   Risner Janiczek, Jessica R ^b   Holt, Jeffrey R ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL;

129 MOUSE; ACTION POTENTIAL; ANIMAL; KNOCKOUT MOUSE; MECHANOTRANSDUCTION; MOUSE; NEWBORN; PHYSIOLOGY; SPIRAL GANGLION; VESTIBULE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; HYPERPOLARIZATION-ACTIVATED CYCLIC NUCLEOTIDE-GATED CHANNELS; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; SPIRAL GANGLION; VESTIBULE, LABYRINTH;

EID: 84897049524     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201311126     Document Type: Article

References (49)

1. Almanza, A., E. Luis, F. Mercado, R. Vega, and E. Soto. 2012. Molecular identity, ontogeny, and cAMP modulation of the hyperpolarizationactivated current in vestibular ganglion neurons. J. Neurophysiol. 108:2264-2275. http://dx.doi.org/10.1152/jn.00337.2012
2. Assad, J.A., G.M. Shepherd, and D.P. Corey. 1991. Tip-link integrity and mechanical transduction in vertebrate hair cells. Neuron. 7:985-994. http://dx.doi.org/10.1016/0896-6273(91)90343-X
3. Baird, R.A., G. Desmadryl, C. Fernández, and J.M. Goldberg. 1988. The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J. Neurophysiol. 60:182-203.
4. BoSmith, R.E., I. Briggs, and N.C. Sturgess. 1993. Inhibitory actions of ZENECA ZD7288 on whole-cell hyperpolarization activated inward current (If) in guinea-pig dissociated sinoatrial node cells. Br. J. Pharmacol. 110:343-349. http://dx.doi.org/10.1111/j.1476-5381.1993.tb13815.x
5. Boyle, R., R.D. Rabbitt, and S.M. Highstein. 2009. Efferent control of hair cell and afferent responses in the semicircular canals. J. Neurophysiol. 102:1513-1525. http://dx.doi.org/10.1152/jn.91367.2008
6. h) current in mouse vestibular primary neurons. Neuroreport. 12:2701-2704. http://dx.doi.org/10.1097/00001756-200108280-00022
7. Chambard, J.M., and J.F. Ashmore. 2005. Regulation of the voltage-gated potassium channel KCNQ4 in the auditory pathway. Pflugers Arch. 450:34-44. http://dx.doi.org/10.1007/s00424-004-1366-2
8. Chan, C.S., R. Shigemoto, J.N. Mercer, and D.J. Surmeier. 2004. HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J. Neurosci. 24:9921-9932. http://dx.doi.org/10.1523/JNEUROSCI.2162-04.2004
9. Chan, C.S., K.E. Glajch, T.S. Gertler, J.N. Guzman, J.N. Mercer, A.S. Lewis, A.B. Goldberg, T. Tkatch, R. Shigemoto, S.M. Fleming, et al. 2011. HCN channelopathy in external globus pallidus neurons in models of Parkinson's disease. Nat. Neurosci. 14:85-92. http://dx.doi.org/10.1038/nn.2692
10. Dhawan, R., S.E. Mann, F.L. Meredith, and K.J. Rennie. 2010. K+ currents in isolated vestibular afferent calyx terminals. J. Assoc. Res. Otolaryngol. 11:463-476. http://dx.doi.org/10.1007/s10162-010-0213-8
11. Dulon, D., S. Safieddine, S.M. Jones, and C. Petit. 2009. Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. J. Neurosci. 29:10474-10487. http://dx.doi.org/10.1523/JNEUROSCI.1009-09.2009
12. Eatock, R.A., and J.E. Songer. 2011. Vestibular hair cells and afferents: two channels for head motion signals. Annu. Rev. Neurosci. 34:501-534. http://dx.doi.org/10.1146/annurev-neuro-061010-113710
13. h ensures high-fidelity dendritic spike responses of motion-sensitive neurons in rat superior colliculus. J. Neurophysiol. 99:2066-2076. http://dx.doi.org/10.1152/jn.00556.2007
14. Géléoc, G.S., J.R. Risner, and J.R. Holt. 2004. Developmental acquisition of voltage-dependent conductances and sensory signaling in hair cells of the embryonic mouse inner ear. J. Neurosci. 24:11148-11159. http://dx.doi.org/10.1523/JNEUROSCI.2662-04.2004
15. Goldberg, J.M. 2000. Afferent diversity and the organization of central vestibular pathways. Exp. Brain Res. 130:277-297. http://dx.doi.org/10.1007/s002210050033
16. Goldberg, J.M., and C. Fernández. 1977. Conduction times and background discharge of vestibular afferents. Brain Res. 122:545-550. http://dx.doi.org/10.1016/0006-8993(77)90465-6
17. Goldberg, J.M., C.E. Smith, and C. Fernández. 1984. Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. J. Neurophysiol. 51:1236-1256.
18. Goldberg, J.M., G. Desmadryl, R.A. Baird, and C. Fernández. 1990. The vestibular nerve of the chinchilla. IV. Discharge properties of utricular afferents. J. Neurophysiol. 63:781-790.
19. Hirvonen, T.P., L.B. Minor, T.E. Hullar, and J.P. Carey. 2005. Effects of Intratympanic Gentamicin on Vestibular Afferents and Hair Cells in the Chinchilla. J. Neurophysiol. 93:643-655. http://dx.doi.org/10.1152/jn.00160.2004
20. Holt, J.R., D.P. Corey, and R.A. Eatock. 1997. Mechanoelectrical transduction and adaptation in hair cells of the mouse utricle, a low-frequency vestibular organ. J. Neurosci. 17:8739-8748.
21. Horwitz, G.C., A. Lelli, G.S. Géléoc, and J.R. Holt. 2010. HCN channels are not required for mechanotransduction in sensory hair cells of the mouse inner ear. PLoS ONE. 5:e8627. http://dx.doi.org/10.1371/journal.pone.0008627
22. Horwitz, G.C., J.R. Risner-Janiczek, S.M. Jones, and J.R. Holt. 2011. HCN channels expressed in the inner ear are necessary for normal balance function. J. Neurosci. 31:16814-16825. http://dx.doi.org/10.1523/JNEUROSCI.3064-11.2011
23. Hudspeth, A.J. 1989. How the ear's works work. Nature. 341:397-404. http://dx.doi.org/10.1038/341397a0
24. Hurley, K.M., S. Gaboyard, M. Zhong, S.D. Price, J.R. Wooltorton, A. Lysakowski, and R.A. Eatock. 2006. M-like K+ currents in type I hair cells and calyx afferent endings of the developing rat utricle. J. Neurosci. 26:10253-10269. http://dx.doi.org/10.1523/JNEUROSCI.2596-06.2006
25. Jagger, D.J., and J.F. Ashmore. 1999. The fast activating potassium current, IK, f, in guinea-pig inner hair cells is regulated by protein kinase A. Neurosci. Lett. 263:145-148. http://dx.doi.org/10.1016/S0304-3940(99)00128-7
26. Kalluri, R., J. Xue, and R.A. Eatock. 2010. Ion channels set spike timing regularity of mammalian vestibular afferent neurons. J. Neurophysiol. 104:2034-2051. http://dx.doi.org/10.1152/jn.00396.2010
27. Kim, Y.H., and J.R. Holt. 2013. Functional contributions of HCN channels in the primary auditory neurons of the mouse inner ear. J. Gen. Physiol. 142:207-223. http://dx.doi.org/10.1085/jgp.201311019
28. Lasker, D.M., G.C. Han, H.J. Park, and L.B. Minor. 2008. Rotational responses of vestibular-nerve afferents innervating the semicircular canals in the C57BL/6 mouse. J. Assoc. Res. Otolaryngol. 9:334-348. http://dx.doi.org/10.1007/s10162-008-0120-4
29. Lelli, A., P. Kazmierczak, Y. Kawashima, U. Müller, and J.R. Holt. 2010. Development and regeneration of sensory transduction in auditory hair cells requires functional interaction between cadherin-23 and protocadherin-15. J. Neurosci. 30:11259-11269. http://dx.doi.org/10.1523/JNEUROSCI.1949-10.2010
30. Levin, M.E., and J.R. Holt. 2012. The function and molecular identity of inward rectifier channels in vestibular hair cells of the mouse inner ear. J. Neurophysiol. 108:175-186. http://dx.doi.org/10.1152/jn.00098.2012
31. Lim, R., A.E. Kindig, S.W. Donne, R.J. Callister, and A.M. Brichta. 2011. Potassium accumulation between type I hair cells and calyx terminals in mouse crista. Exp. Brain Res. 210:607-621. http://dx.doi.org/10.1007/s00221-011-2592-4
32. Ludwig, A., X. Zong, J. Stieber, R. Hullin, F. Hofmann, and M. Biel. 1999. Two pacemaker channels from human heart with profoundly different activation kinetics. EMBO J. 18:2323-2329. http://dx.doi.org/10.1093/emboj/18.9.2323
33. Ludwig, A., T. Budde, J. Stieber, S. Moosmang, C. Wahl, K. Holthoff, A. Langebartels, C. Wotjak, T. Munsch, X. Zong, et al. 2003. Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2. EMBO J. 22:216-224. http://dx.doi.org/10.1093/emboj/cdg032
34. Lysakowski, A., S. Gaboyard-Niay, I. Calin-Jageman, S. Chatlani, S.D. Price, and R.A. Eatock. 2011. Molecular microdomains in a sensory terminal, the vestibular calyx ending. J. Neurosci. 31:10101-10114. http://dx.doi.org/10.1523/JNEUROSCI.0521-11.2011
35. h normalizes temporal summation in hippocampal CA1 neurons. Nat. Neurosci. 2:508-514. http://dx.doi.org/10.1038/9158
36. Marquis, R.E., and A.J. Hudspeth. 1997. Effects of extracellular Ca2+ concentration on hair-bundle stiffness and gating-spring integrity in hair cells. Proc. Natl. Acad. Sci. USA. 94:11923-11928. http://dx.doi.org/10.1073/pnas.94.22.11923
37. h) in vestibular calyx terminals: characterization and role in shaping postsynaptic events. J. Assoc. Res. Otolaryngol. 13:745-758. http://dx.doi.org/10.1007/s10162-012-0342-3
38. Narayanan, R., and D. Johnston. 2007. Long-term potentiation in rat hippocampal neurons is accompanied by spatially widespread changes in intrinsic oscillatory dynamics and excitability. Neuron. 56:1061-1075. http://dx.doi.org/10.1016/j.neuron.2007.10.033
39. Nolan, M.F., G. Malleret, K.H. Lee, E. Gibbs, J.T. Dudman, B. Santoro, D. Yin, R.F. Thompson, S.A. Siegelbaum, E.R. Kandel, and A. Morozov. 2003. The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells. Cell. 115:551-564. http://dx.doi.org/10.1016/S0092-8674(03)00884-5
40. Pattnaik, B.R., and B.A. Hughes. 2012. Effects of KCNQ channel modulators on the M-type potassium current in primate retinal pigment epithelium. Am. J. Physiol. Cell Physiol. 302:C821-C833. http://dx.doi.org/10.1152/ajpcell.00269.2011
41. Rennie, K.J., and M.A. Streeter. 2006. Voltage-Dependent Currents in Isolated Vestibular Afferent Calyx Terminals. J. Neurophysiol. 95:26-32. http://dx.doi.org/10.1152/jn.00641.2005
42. Risner, J.R., and J.R. Holt. 2006. Heterogeneous potassium conductances contribute to the diverse firing properties of postnatal mouse vestibular ganglion neurons. J. Neurophysiol. 96:2364-2376. http://dx.doi.org/10.1152/jn.00523.2006
43. Rüsch, A., A. Lysakowski, and R.A. Eatock. 1998. Postnatal development of type I and type II hair cells in the mouse utricle: acquisition of voltage-gated conductances and differentiated morphology. J. Neurosci. 18:7487-7501.
44. Santoro, B., S. Chen, A. Luthi, P. Pavlidis, G.P. Shumyatsky, G.R. Tibbs, and S.A. Siegelbaum. 2000. Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J. Neurosci. 20:5264-5275.
45. Songer, J.E., and R.A. Eatock. 2013. Tuning and timing in mammalian type I hair cells and calyceal synapses. J. Neurosci. 33:3706-3724. http://dx.doi.org/10.1523/JNEUROSCI.4067-12.2013
46. Sousa, A.D., L.R. Andrade, F.T. Salles, A.M. Pillai, E.D. Buttermore, M.A. Bhat, and B. Kachar. 2009. The septate junction protein caspr is required for structural support and retention of KCNQ4 at calyceal synapses of vestibular hair cells. J. Neurosci. 29:3103-3108. http://dx.doi.org/10.1523/JNEUROSCI.4868-08.2009
47. Trapani, J.G., and T. Nicolson. 2011. Mechanism of spontaneous activity in afferent neurons of the zebrafish lateral-line organ. J. Neurosci. 31:1614-1623. http://dx.doi.org/10.1523/JNEUROSCI.3369-10.2011
48. Wu, X., L. Liao, X. Liu, F. Luo, T. Yang, and C. Li. 2012. Is ZD7288 a selective blocker of hyperpolarization-activated cyclic nucleotidegated channel currents? Channels (Austin). 6:438-442. http://dx.doi.org/10.4161/chan.22209
49. Yi, E., I. Roux, and E. Glowatzki. 2010. Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. J. Neurophysiol. 103:2532-2543. http://dx.doi.org/10.1152/jn.00506.2009