Skip to main content
Log in

Postnatal Expression of an Apamin-Sensitive K(Ca) Current in Vestibular Calyx Terminals

  • Published:
The Journal of Membrane Biology Aims and scope Submit manuscript

Abstract

Afferent innervation patterns in the vestibular periphery are complex, and vestibular afferents show a large variation in their regularity of firing. Calyx fibers terminate on type I vestibular hair cells and have firing characteristics distinct from the bouton fibers that innervate type II hair cells. Whole-cell patch clamp was used to investigate ionic currents that could influence firing patterns in calyx terminals. Underlying K(Ca) conductances have been described in vestibular ganglion cells, but their presence in afferent terminals has not been investigated previously. Apamin, a selective blocker of SK-type calcium-activated K+ channels, was tested on calyx afferent terminals isolated from gerbil semicircular canals during postnatal days 1–50. Lowering extracellular calcium or application of apamin (20–500 nM) reduced slowly activating outward currents in voltage clamp. Apamin also reduced the action potential afterhyperpolarization (AHP) in whole-cell current clamp, but only after the first two postnatal weeks. K+ channel expression increased during the first postnatal month, and SK channels were found to contribute to the AHP, which may in turn influence discharge regularity in calyx vestibular afferents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • 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 neurons. J Physiol 567:67–78

    Article  PubMed  CAS  Google Scholar 

  • Baird RA, Desmadryl G, Fernández C, Goldberg JM (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

    PubMed  CAS  Google Scholar 

  • Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8:451–465

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Chabbert C, Chambard JM, Valmier J, Sans A, Desmadryl G (2001b) Hyperpolarization-activated (I h) current in mouse vestibular primary neurons. Neuroreport 12:2701–2704

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Curthoys IS (1979) The development of function of horizontal semicircular canal primary neurons in the rat. Brain Res 167:41–52

    Article  PubMed  CAS  Google Scholar 

  • Curthoys IS (1982) Postnatal developmental changes in the response of rat primary horizontal semicircular canal neurons to sinusoidal angular accelerations. Exp Brain Res 47:295–300

    PubMed  CAS  Google Scholar 

  • Curti S, Gómez L, Budelli R, Pereda AE (2008) Subthreshold sodium current underlies essential functional specializations at primary auditory afferents. J Neurophysiol 99:1683–1699

    Article  PubMed  Google Scholar 

  • Desai SS, Zeh C, Lysakowski A (2005) Comparative morphology of rodent vestibular periphery. I. Saccular and utricular maculae. J Neurophysiol 93:251–266

    Article  PubMed  Google Scholar 

  • Desmadryl G, Raymond J, Sans A (1986) In vitro electrophysiological study of spontaneous activity in neonatal mouse vestibular ganglion neurons during development. Brain Res 390:133–136

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Dhawan R, Mann SE, Meredith FL, Rennie KJ (2010) K+ currents in isolated vestibular afferent calyx terminals. J Assoc Res Otolaryngol 11:463–476

    Article  PubMed  Google Scholar 

  • Dutia MB, Johnston AR (1998) Development of action potentials and apamin-sensitive after-potentials in mouse vestibular nucleus neurons. Exp Brain Res 118:148–154

    Article  PubMed  CAS  Google Scholar 

  • Eatock RA, Hurley KM (2003) Functional development of hair cells. Curr Top Dev Biol 57:389–448

    Article  PubMed  Google Scholar 

  • Fernández C, Baird RA, Goldberg JM (1988) The vestibular nerve of the chinchilla. I. Peripheral innervation patterns in horizontal and superior semicircular canals. J Neurophysiol 60:167–181

    PubMed  Google Scholar 

  • Gamper N, Shapiro MS (2003) Calmodulin mediates Ca2+-dependent modulation of M-type K+ channels. J Gen Physiol 122:17–31

    Article  PubMed  CAS  Google Scholar 

  • Geier P, Lagler M, Boehm S, Kubista H (2011) Dynamic interplay of excitatory and inhibitory coupling modes of neuronal L-type calcium channels. Am J Physiol Cell Physiol 300:C937–C949

    Article  PubMed  CAS  Google Scholar 

  • Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5:147–154

    Article  PubMed  CAS  Google Scholar 

  • Goldberg JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brain Res 130:277–297

    Article  PubMed  CAS  Google Scholar 

  • Hullar TE, Della Santina CC, Hirvonen T, Lasker DM, Carey JP, Minor LB (2005) Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. J Neurophysiol 93:2777–2786

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Iwasaki S, Chihara Y, Komuta Y, Ito K, Sahara Y (2008) Low-voltage-activated potassium channels underlie the regulation of intrinsic firing properties of rat vestibular ganglion cells. J Neurophysiol 100:2192–2204

    Article  PubMed  CAS  Google Scholar 

  • Kalluri R, Xue J, Eatock RA (2010) Ion channels set spike timing regularity of mammalian vestibular afferent neurons. J Neurophysiol 104:2034–2051

    Article  PubMed  Google Scholar 

  • Leonard RB, Kevetter GA (2002) Molecular probes of the vestibular nerve. I Peripheral termination patterns of calretinin, calbindin and peripherin containing fibers. Brain Res 928:8–17

    Article  PubMed  CAS  Google Scholar 

  • Li G, Meredith FL, Rennie KJ (2010) Development of K+ and Na+ conductances in rodent postnatal semicircular canal type I hair cells. Am J Physiol Regul Integr Comp Physiol 298:R351–R358

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Lysakowski A, Minor LB, Fernández C, Goldberg JM (1995) Physiological identification of morphologically distinct afferent classes innervating the cristae ampullares of the squirrel monkey. J Neurophysiol 73:1270–1281

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Marcotti W, Johnson SL, Kros CJ (2004) A transiently expressed SK current sustains and modulates action potential activity in immature mouse inner hair cells. J Physiol 560:691–708

    Article  PubMed  CAS  Google Scholar 

  • Monaghan AS, Benton DC, Bahia PK, Hosseini R, Shah YA, Haylett DG, Moss GW (2004) The SK3 subunit of small conductance Ca2+-activated K+ channels interacts with both SK1 and SK2 subunits in a heterologous expression system. J Biol Chem 279:1003–1009

    Article  PubMed  CAS  Google Scholar 

  • Nie L, Zhu J, Gratton MA, Liao A, Mu KJ, Nonner W, Richardson GP, Yamoah EN (2008) Molecular identity and functional properties of a novel T-type Ca2+ channel cloned from the sensory epithelia of the mouse inner ear. J Neurophysiol 100:2287–2299

    Article  PubMed  CAS  Google Scholar 

  • Pérez C, Limón A, Vega R, Soto E (2009) The muscarinic inhibition of the potassium M-current modulates the action-potential discharge in the vestibular primary-afferent neurons of the rat. Neuroscience 158:1662–1674

    Article  PubMed  Google Scholar 

  • Pyott SJ, Meredith AL, Fodor AA, Vázquez AE, Yamoah EN, Aldrich RW (2007) Cochlear function in mice lacking the BK channel alpha, beta1, or beta4 subunits. J Biol Chem 282:3312–3324

    Article  PubMed  CAS  Google Scholar 

  • Rennie KJ, Correia MJ (1994) Potassium currents in mammalian and avian isolated type I semicircular canal hair cells. J Neurophysiol 71:317–329

    PubMed  CAS  Google Scholar 

  • Rennie KJ, Streeter MA (2006) Voltage-dependent currents in isolated vestibular afferent calyx terminals. J Neurophysiol 95:26–32

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Rocha-Sanchez SMS, Morris KA, Kachar B, Nichols D, Fritzsch B, Beisel KW (2007) Developmental expression of Kcnq4 in vestibular neurons and neurosensory epithelia. Brain Res 1139:117–125

    Article  PubMed  CAS  Google Scholar 

  • Rüsch A, Eatock RA (1996) A delayed rectifier conductance in type I hair cells of the mouse utricle. J Neurophysiol 76:995–1004

    PubMed  Google Scholar 

  • Sah P, Faber ES (2002) Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol 66:345–353

    Article  PubMed  CAS  Google Scholar 

  • Saito Y, Takazawa T, Ozawa S (2008) Relationship between after-hyperpolarization profiles and the regularity of spontaneous firings in rat medial vestibular nucleus neurons. Eur J Neurosci 28:288–298

    Article  PubMed  Google Scholar 

  • Schweizer FE, Savin D, Luu C, Sultemeier DR, Hoffman LF (2009) Distribution of high-conductance calcium-activated potassium channels in rat vestibular epithelia. J Comp Neurol 517:134–145

    Article  PubMed  CAS  Google Scholar 

  • Smith CE, Goldberg JM (1986) A stochastic after-hyperpolarization model of repetitive activity in vestibular afferents. Biol Cybern 54:41–51

    Article  PubMed  CAS  Google Scholar 

  • Smith MR, Nelson AB, Du Lac S (2002) Regulation of firing response gain by calcium-dependent mechanisms in vestibular nucleus neurons. J Neurophysiol 87:2031–2042

    PubMed  Google Scholar 

  • Szatanik M, Vibert N, Vassias I, Guénet JL, Eugène D, de Waele C, Jaubert J (2008) Behavioral effects of a deletion in Kcnn2, the gene encoding the SK2 subunit of small-conductance Ca2+-activated K+ channels. Neurogenetics 9:237–248

    Article  PubMed  CAS  Google Scholar 

  • Weisz C, Glowatzki E, Fuchs P (2009) The postsynaptic function of type II cochlear afferents. Nature 461:1126–1129

    Article  PubMed  CAS  Google Scholar 

  • Xu T, Nie L, Zhang Y, Mo J, Feng W, Wei D, Petrov E, Calisto LE, Kachar B, Beisel KW, Vazquez AE, Yamoah EN (2007) Roles of alternative splicing in the functional properties of inner ear-specific KCNQ4 channels. J Biol Chem 282:23899–23909

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This study was supported by National Institute on Deafness and Other Communication Disorders (NIDCD) grant DC-008297 and an American Otological Society grant to K. J. R. F. L. M. was partly supported by 5T32NS007083. The authors thank Tommy Bui for excellent technical help and Scott Mann for comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katherine J. Rennie.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meredith, F.L., Li, G.Q. & Rennie, K.J. Postnatal Expression of an Apamin-Sensitive K(Ca) Current in Vestibular Calyx Terminals. J Membrane Biol 244, 81–91 (2011). https://doi.org/10.1007/s00232-011-9400-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00232-011-9400-8

Keywords

Navigation