全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2014 

Physiological Characterization of Vestibular Efferent Brainstem Neurons Using a Transgenic Mouse Model

DOI: 10.1371/journal.pone.0098277

Full-Text   Cite this paper   Add to My Lib

Abstract:

The functional role of efferent innervation of the vestibular end-organs in the inner ear remains elusive. This study provides the first physiological characterization of the cholinergic vestibular efferent (VE) neurons in the brainstem by utilizing a transgenic mouse model, expressing eGFP under a choline-acetyltransferase (ChAT)-locus spanning promoter in combination with targeted patch clamp recordings. The intrinsic electrical properties of the eGFP-positive VE neurons were compared to the properties of the lateral olivocochlear (LOC) brainstem neurons, which gives rise to efferent innervation of the cochlea. Both VE and the LOC neurons were marked by their negative resting membrane potential <?75 mV and their passive responses in the hyperpolarizing range. In contrast, the response properties of VE and LOC neurons differed significantly in the depolarizing range. When injected with positive currents, VE neurons fired action potentials faithfully to the onset of depolarization followed by sparse firing with long inter-spike intervals. This response gave rise to a low response gain. The LOC neurons, conversely, responded with a characteristic delayed tonic firing upon depolarizing stimuli, giving rise to higher response gain than the VE neurons. Depolarization triggered large TEA insensitive outward currents with fast inactivation kinetics, indicating A-type potassium currents, in both the inner ear-projecting neuronal types. Immunohistochemistry confirmed expression of Kv4.3 and 4.2 ion channel subunits in both the VE and LOC neurons. The difference in spiking responses to depolarization is related to a two-fold impact of these transient outward currents on somatic integration in the LOC neurons compared to in VE neurons. It is speculated that the physiological properties of the VE neurons might be compatible with a wide-spread control over motion and gravity sensation in the inner ear, providing likewise feed-back amplification of abrupt and strong phasic signals from the semi-circular canals and of tonic signals from the gravito-sensitive macular organs.

References

[1]  Aschoff A, Ostwald J (1987) Different origins of cochlear efferents in some bat species, rats, and guinea pigs. J Comp Neurol 264: 56–72. doi: 10.1002/cne.902640106
[2]  Adam TJ, Schwarz DWF, Finlayson PG (1999) Firing properties of chopper and delay neurons in the lateral superior olive of the rat. Exp Brain Res 124: 489–502. doi: 10.1007/s002210050645
[3]  Birinyi A, Straka H, Matesz C, Dieringer N (2001) Location of dye-coupled second order and of efferent vestibular neurons labeled from individual semicircular canal or otolith organs in the frog. Brain Res 921: 44–59. doi: 10.1016/s0006-8993(01)03075-x
[4]  Birnbaum SG, Varga AW, Yuan L, Anderson AE, Sweatt D, et al. (2004) Structure and function of Kv4-family transient potassium channels. Physiol Rev 84: 803–833. doi: 10.1152/physrev.00039.2003
[5]  Boyle R, Highstein SM (1990) Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents. J Neurosci 10: 1570–1582.
[6]  Boyle R, Rabbitt RD, Highstein SM (2009) Efferent control of hair cell and afferent responses in the semicircular canals. J Neurophysiol 102: 1513–1525. doi: 10.1152/jn.91367.2008
[7]  Brown MC (1993) Fiber pathways and branching patterns of biocytin-labeled olivocochlear neurons in the mouse brainstem. J Comp Neurol 337: 600–13. doi: 10.1002/cne.903370406
[8]  Brown DA, Adams PR (1980) Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283: 673–676. doi: 10.1038/283673a0
[9]  Brown MC, Levine JL (2008) Dendrites of medial olivocochlear neurons in mouse. Neuroscience 154: 147–59. doi: 10.1016/j.neuroscience.2007.12.045
[10]  Campbell JP, Henson MM (1988) Olivocochlear neurons in the brainstem of the mouse. Hear Res 35: 271–274. doi: 10.1016/0378-5955(88)90124-4
[11]  Carpenter MB, Chang L, Pereira AB, Hersh LB, Bruce G, et al. (1987) Vestibular and cochlear efferent neurons in the monkey identified by immunocytochemical methods. Brain Res 408: 275–80. doi: 10.1016/0006-8993(87)90387-8
[12]  Castellano-Mu?oz M, Israel SH, Hudspeth AJ (2010) Efferent control of the electrical and mechanical properties of hair cells in the bullfrog's sacculus. PLOS One 5: e13777. doi: 10.1371/journal.pone.0013777
[13]  Chen X, Johnston D (2004) Properties of single voltage-dependent K+ channels in dendrites of CA1 pyramidal neurones of rat hippocampus. J Physiol 559: 187–203. doi: 10.1113/jphysiol.2004.068114
[14]  Chi FL, Jiao Y, Liu HJ, Wang J, Shi Y, et al. (2007) Retrograde neuron tracing with microspheres reveals projection of CGRP-immunolabeled vestibular afferent neurons to the vestibular efferent nucleus in the brainstem of rats. Neuroendocrinol 85: 131–138. doi: 10.1159/000101959
[15]  Connor JA, Stevens CF (1971) Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J Physiol 213: 21–30.
[16]  Cooper NP, Guinan JJ Jr (2006) Efferent-mediated control of basilar membrane motion. J Physiol 576: 49–54. doi: 10.1113/jphysiol.2006.114991
[17]  Cullen KE, Minor LB (2002) Semicircular canal afferents similarly encode active and passive head-on-body rotations: implications for the role of vestibular efference. J Neurosci 22: RC226.
[18]  Darrow KN, Maison SF, Liberman MC (2006) Cochlear efferent feedback balances interaural sensitivity. Nat Neurosci 12: 1474–1476. doi: 10.1038/nn1807
[19]  Dodson PD, Forsythe ID (2004) Presynaptic K+ potassium channels: electrifying regulators of synaptic terminal excitability. Trends Neurosci 27: 210–217. doi: 10.1016/j.tins.2004.02.012
[20]  Felix RA 2nd, Vonderschen K, Berrebi AS, Magnusson AK (2013) Development of on-off spiking in superior paraolivary nucleus neurons of the mouse. J Neurophysiol 109: 2691–704. doi: 10.1152/jn.01041.2012
[21]  Fitzakerley JL, Star KV, Rinn JL, Elmquist BJ (2000) Expression of Shal potassium channel subunits in the adult and developing cochlear nucleus of the mouse. Hear Res 147: 31–45. doi: 10.1016/s0378-5955(00)00118-0
[22]  Fujino K, Koyano K, Ohmori H (1997) Lateral and medial olivocochlear neurons have distinct electrophysiological properties in the rat brain slice. J Neurophysiol 77: 2788–2804.
[23]  Gacek RR (1969) The course and central termination of first order neurons supplying the vestibular end organs in the cat. Acta Otolaryngol Suppl 254: 1–66.
[24]  Gacek RR, Lyon M (1974) The localization of vestibular efferent neurons in the kitten with horseradish peroxidase. Acta Otolaryngol 77: 92–101. doi: 10.3109/00016487409124603
[25]  Goldberg JM, Fernández C (1980) Efferent vestibular system in the squirrel monkey: anatomical location and influence on afferent activity. J Neurophysiol 43: 986–1025.
[26]  Highstein SM (1992) The efferent control of the organs of balance and equilibrium in the toadfish, Opsanus tau. Ann N Y Acad Sci 656: 108–123. doi: 10.1111/j.1749-6632.1992.tb25203.x
[27]  Highstein SM, Baker R (1985) Action of the efferent vestibular system on primary afferents in the toadfish, Opsanus tau. J Neurophysiol 54: 370–84.
[28]  Highstein SM, Baker R (1986) Organization of the efferent vestibular nuclei and nerves of the toadfish, Opsanus tau. J Comp Neurol 243: 309–325. doi: 10.1002/cne.902430303
[29]  Holt JC, Lysakowski A, Goldberg JM (2006) Mechanisms of efferent-mediated responses in the turtle posterior crista. J Neurosci 26: 13180–13193. doi: 10.1523/jneurosci.3539-06.2006
[30]  Jacob RG, Furman JM (2001) Psychiatric consequences of vestibular dysfunction. Curr Opin Neurol 14: 41–46. doi: 10.1097/00019052-200102000-00007
[31]  Jamali M, Sadeghi SG, Cullen KE (2009) Response of vestibular nerve afferents innervating utricle and saccule during passive and active translations. J Neurophysiol 101: 141–149. doi: 10.1152/jn.91066.2008
[32]  Jerng HH, Shahidullah M, Covarrubias M (1999) Inactivation gating of Kv4 potassium channels: molecular interactions involving the inner vestibule of the pore. J Gen Physiol 113: 641–660. doi: 10.1085/jgp.113.5.641
[33]  Johnston J, Griffin SJ, Baker C, Forsythe ID (2008) Kv4 (A-type) potassium currents in the mouse medial nucleus of the trapezoid body. Eur J Neurosci 27: 1391–1399. doi: 10.1111/j.1460-9568.2008.06116.x
[34]  Korte GE (1979) The brainstem projection of the vestibular nerve in the cat. J Comp Neurol 184: 279–292. doi: 10.1002/cne.901840205
[35]  Lasker DM, Han GC, Park HJ, Minor LB (2008) Rotational responses of vestibular-nerve afferents innervating the semicircular canals in the C57BL/6 mouse. J Assoc Res Otolaryngol 9: 334–348. doi: 10.1007/s10162-008-0120-4
[36]  Lendvai B, Halmos GB, Polony G, Kapocsi J, Horváth T, et al. (2011) Chemical neuroprotection in the cochlea: the modulation of dopamine release from lateral olivocochlear efferents. Neurochem Int 59: 150–8. doi: 10.1016/j.neuint.2011.05.015
[37]  Li YP, Baskin F, Davis R, Hersh LB (1993) Cholinergic neuron-specific expression of the human choline acetyltransferase gene is controlled by silencer elements. J Neurochem 61: 748–751. doi: 10.1111/j.1471-4159.1993.tb02181.x
[38]  Li C, Zhang YK, Guan ZL, Shum DK, Chan YS (2005) Vestibular afferent innervation in the vestibular efferent nucleus of rats. Neurosci Lett 385: 36–40. doi: 10.1016/j.neulet.2005.05.024
[39]  Lysakowski A, Goldberg JM (1997) A regional ultrastructural analysis of the cellular and synaptic architecture in the chinchilla cristae ampullares. J Comp Neurol 389: 419–443. doi: 10.1002/(sici)1096-9861(19971222)389:3<419::aid-cne5>3.0.co;2-3
[40]  Lysakowski A, Goldberg JM (2008) Ultrastructural analysis of the cristae ampullares in the squirrel monkey (Saimiri sciureus). J Comp Neurol 511: 47–64. doi: 10.1002/cne.21827
[41]  L?nnerberg P, Lendahl U, Funakoshi H, Arhlund-Richter L, Persson H, et al. (1995) Regulatory region in choline acetyltransferase gene directs developmental and tissue-specific expression in transgenic mice. Proc Natl Acad Sci U S A 92: 4046–4050. doi: 10.1073/pnas.92.9.4046
[42]  Marcus DA, Furman JM, Balaban CD (2005) Motion sickness in migraine sufferers. Expert Opin Pharmacother 6: 2691–2697. doi: 10.1517/14656566.6.15.2691
[43]  Marlinski V, Plotnik M, Goldberg JM (2004) Efferent actions in the chinchilla vestibular labyrinth. J Assoc Res Otolaryngol 5: 126–43. doi: 10.1007/s10162-003-4029-7
[44]  McCrea RA, Gdowski GT, Boyle R, Belton T (1999) Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. J Neurophysiol 82: 416–28.
[45]  McCue MP, Guinan JJ Jr (1994) Influence of efferent stimulation on acoustically responsive vestibular afferents in the cat. J Neurosci 14: 6071–6083.
[46]  Metts BA, Kaufman GD, Perachio AA (2006) Polysynaptic inputs to vestibular efferent neurons as revealed by viral transneuronal tracing. Exp Brain Res 172: 261–274. doi: 10.1007/s00221-005-0328-z
[47]  Minor LB (1998) Physiological principles of vestibular function on earth and in space. Otolaryngol Head Neck Surg 118: S5–15. doi: 10.1016/s0194-5998(98)70002-6
[48]  Misawa H, Ishii K, Deguchi T (1992) Gene expression of mouse choline acetyltransferase. Alternative splicing and identification of a highly active promoter region. J Biol Chem 267: 20392–20399.
[49]  Murakami DM, Erkman L, Hermanson O, Rosenfeld MG, Fuller CA (2002) Evidence for vestibular regulation of autonomic functions in a mouse genetic model. Proc Natl Acad Sci U S A 99: 17078–17082. doi: 10.1073/pnas.252652299
[50]  Naciff JM, Behbehani MM, Misawa H, Dedman JR (1999) Identification and transgenic analysis of a murine promoter that targets cholinergic neuron expression. J Neurochem 72: 17–28. doi: 10.1046/j.1471-4159.1999.0720017.x
[51]  Pape HC (1996) Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu Rev Physiol 58: 299–327. doi: 10.1146/annurev.ph.58.030196.001503
[52]  Plotnik M, Marlinski V, Goldberg JM (2005) Efferent-mediated fluctuations in vestibular nerve discharge: a novel, positive-feedback mechanism of efferent control. J Assoc Res Otolaryngol 6: 311–323. doi: 10.1007/s10162-005-0010-y
[53]  Purcell IM, Perachio AA (1997) Three-dimensional analysis of vestibular efferent neurons innervating semicircular canals of the gerbil. J Neurophysiol 78: 3234–3348.
[54]  Rabbit RD, Brownell WE (2011) Efferent modulation of hair cell function. Current Opin Otolaryngol and Head and Neck Surg 19: 376–81. doi: 10.1097/moo.0b013e32834a5be1
[55]  Raphael Y, Altschuler RA (2003) Structure and innervation of the cochlea. Brain Res Bull 60: 397–422. doi: 10.1016/s0361-9230(03)00047-9
[56]  Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21: 2131–42.
[57]  Rusznák Z, Bakondi G, Pocsai K, Pór A, Kosztka L, et al. (2008) Voltage-gated potassium channel (Kv) subunits expressed in the rat cochlear nucleus. J Histochem Cytochem 56: 443–65. doi: 10.1369/jhc.2008.950303
[58]  Sadeghi SG, Minor LB, Cullen KE (2007) Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy. J Neurophysiol 97: 1503–1514. doi: 10.1152/jn.00829.2006
[59]  Sadeghi SG, Goldberg JM, Minor LB, Cullen KE (2009) Efferent-mediated responses in vestibular nerve afferents of the alert macaque. J Neurophysiol 101: 988–1001. doi: 10.1152/jn.91112.2008
[60]  Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29: 467–492.
[61]  Serodio P, Rudy B (1998) Differential expression of Kv4 K+ channel subunits mediating subthreshold transient K+ (A-type) currents in rat brain. J Neurophysiol 79: 1081–1091.
[62]  Sterenborg JC, Pilati N, Sheridan CJ, Uchitel OD, Forsythe ID, et al. (2010) Lateral olivocochlear (LOC) neurons of the mouse LSO receive excitatory and inhibitory synaptic inputs with slower kinetics than LSO principal neurons. Hear Res 270: 119–26. doi: 10.1016/j.heares.2010.08.013
[63]  Storm JF (1988) Temporal integration by a slowly inactivating K+ current in hippocampal neurons. Nature 336: 379–381. doi: 10.1038/336379a0
[64]  Storm JF (1989) An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. J Physiol 409: 171–90.
[65]  Svirskis G, Kotak V, Sanes DH, Rinzel J (2002) Enhancement of signal-to-noise ratio and phase locking for small inputs by a low-threshold outward current in auditory neurons. J Neurosci 22: 11019–11025.
[66]  Tallini YN, Shui B, Greene KS, Deng K-Y, Doran R, et al. (2006) BAC transgenic mice express enhanced green fluorescent protein in central and peripheral cholinergic neurons. Physiol Gen 27: 391–397. doi: 10.1152/physiolgenomics.00092.2006
[67]  Trifonov S, Houtani T, Hamada S, Kase M, Maruyama M, et al. (2009) In situ hybridization study of the distribution of choline acetyltransferase mRNA and its splice variants in the mouse brain and spinal cord. Neurosci 159: 344–357. doi: 10.1016/j.neuroscience.2008.12.054
[68]  Tzingounis AV, Nicoll RA (2008) Contribution of KCNQ2 and KCNQ3 to the medium and slow afterhyperpolarization currents. Proc Natl Acad Sci U S A 105: 19974–19979. doi: 10.1073/pnas.0810535105
[69]  Yao W, Godfrey DA (1998) Immunohistochemical evaluation of cholinergic neurons in the rat superior olivary complex. Microsc Res and Tech 41: 270–283. doi: 10.1002/(sici)1097-0029(19980501)41:3<270::aid-jemt10>3.0.co;2-l
[70]  Yuan W, Burkhalter A, Nerbonne JM (2005) Functional role of the fast transient outward K+current IA in pyramidal neurons in (rat) primary visual cortex. J Neurosci 25: 9185–9194. doi: 10.1523/jneurosci.2858-05.2005

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133